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Annals of the
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Volume 91, Number 1
April 2004

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This paper

д MN еа i

48 ( ce of Paper).

Volume 91 Annals
Number 1 of the
2004 Missouri

Botanical

Garden

A REVISION OF TRISETUM. Victor L. Finot,” Paul M. Peterson,“
PEYRITSCHIA, AND 1 Soreng,? and Fernando О.
SPHENOPHOLIS (POACEAE:

POOIDEAE: AVENINAE) IN

MEXICO AND CENTRAL

AMERICA

ABSTRACT

A taxonomic treatment of Trisetum, Peyritschia, and Sphe 8 for Mexico and Central Americ a is given. In Mexico
and Central America four species of Peyritschia. two species of | ie ded and 17 species of Trisetum s. str. are
recognized. Peyritschia deyeuxioides and F P. pringlei range E Mexico to Ecuador, P. koelerioides i is found in southern
lexico to Guate зне and P. humilis is mille mic to Mexico. a. е ranges from Canada to es U.S.A.
and Mexico. whereas S. interrupta is found in the southwester nd Baja California, Mexico. Mexico has the
ecies of Trisetum të - found in

—

largest e of Fl species al 15. and nine of these are Five sp
E three in Costa Rica and Panama. and a single species is found i in 1 Honduras and the Dominican Republic.

ew subgenus Deschampsioidea (Louis-Marie) Finot in Trisetum is propi oed. Four new species of Trisetum from
Mexic o are described and illustrated: J. durangense Finot & P. M. Peterson, T. martha- -gonzaleziae P. M. Peterson &
Finot, and J. Ja Hlenbergii Soreng, Finot & P. M. j erson (all in subg. Deschampsioidea ); and T. ба ашм Finot &
Zuloaga (in subg. Trisetum, sect. dar pies Kevs for the genera, subgenera, sections, an id species of Trisetum, Peyr-
itschia, and Си that occur in Mexico а n "entral America are given. The names Trisetum AU E Fourn.
and Trisetum subsect. Desc 5 Louis-Marie are lectotypified.

Key words: Aveninae, Gramineae, Peyritschia, Poaceae, Pooideae, Sphenopholis, Trisetum.

This paper is part of the doctoral thesis of VLF in the Dpto. Botánica. Universidad de Concepción, Concepción.
Chile. We thank Alice Tangerini and 7 Dudás E preparing E illustrations. Thanks to the Directors and
‘urators of the following herbaria: ВАА. BAF. C. CHDIR, CONC, CR, QCA, P. US, S, and SI. We thank Olof Ryding

(Botanical Museum Copenhage n) for sending a xerox of и. type of Deyeuxia gracilis, and Victoria C. Hollowe ll and
an anonymous reviewer for suggesting improvements to the manuse ript. VLF gratefully ac ‘knowledges the Pedersen
Foundation for a fe llowship to КИР types of Trisetum at Paris (Р) апа Stoc 'kholm (S); the MINEDUC for a fellowship
to study types at the Smithsonian Institution. Washington. D.C.. and the Instituto de Botánica deque cs nos Aires;
the financial suka from Dirección de Investigacion, Universidad de Concepción, Project DIUC 201.121.005- L. 0; and
the help of Oscar Matthei and Clodomiro Marticorena (U. de Concepción, Chile) for directing his Ph.D.
2 Unive rsidad de Concepción. Facultad de Agronomía. Dpto. Producción Animal. Casilla 537, Chillan. Chile.
vifinot@udec.cl.
ir epartment of Botany. National Museum of Natural History, Smithsonian Institution, Washington. D.C. 20013-7012,

ra de Botánica Darwinion, Labardén 200, San Isidro 1642, Argentina.

ANN. MISSOURI Bor. GARD. 91: 1-30. 2004.

Annals of the
Missouri Botanical Garden

RESUMEN

Se presenta un tratamiento taxonómic o de los géneros Trisetum, Peyritschia у Sphenopholis para шек у América

Central. Cuatro especies de sch
nocidas en México y Ce Шш гїса. Peyritse hia deye >UXLOL
rioides se encuentra uen el sur
ientra en Canadá, EE.

we

se епс!

de Trisetum se encuentran en Guatemala. tres en Ce

Se propone un nuevo subgénero Desc hampsioide a " ш Меле ») Finot en Trisetum. Cuatro nue

dos especies de Sphenopholis у

йез ур,

México, mientras 5. in terrupta habita el sudoeste de EE.
México. México posee el mayor nümero de especies Е Trisetum, 15 especies, nueve de ellas endémicas. Ci
a Rica y Panamá y sólo una en Honduras y Re públic a Hone 'ana.

. fueron reco-

E koe

17 especies de Trisetum s.

pringlei habitan desde México x e aor

Ub.

у n 1 мис
Inco espec ies

de México son descritas e ilustradas: T. durangense Finot & P. M. Peterson. T. martha-gonzaleziae P. M. Peterson &
Finot y T. spellenbergii Sore ng. Finot & P. M. Peterson (todas en subg. Desc "hampsioidea); v T. ligulatum m & Zuloaga
(en subg. Trisetum, sect. Trisetaera). Se presentan c ru para los géneros, subgéneros, secciones y especies de Trisetum,

Peyritschia y cox bana nr presentes en México у

América Central. Los elie Trisetum gracile Е. ЫШ. у Trisetum

subsect. Desc hampsioidea Louis-Marie fueron lec totipificados.

Trisetum Pers. comprises about 70 species in
temperate regions of Europe, Asia, America, Aus-
tralia, and New Zealand (Louis-Marie, 1928-1929:
Hitchcock, 1939; Swallen, 1948; Tsvelev, 1970.
1983: Jonsell, 1980; Veldkamp & Van der Have,
1983: Clayton & Renvoize, 1986; Pohl & Davidse,
1994, 2002; Edgar, 1998; Soreng et al., 2003). A
general account of the American taxa of Trisetum
was published by Louis-Marie (1928-1929). in
which he recognized a total of 60 species. Hitch-
cock (1939) recognized 19 species of Trisetum in
North There are 38
species of Trisetum in North. Central. and South
America (Finot, 2003b).
ception of the cosmopolitan J. spicatum (L.) K.
Richt.,

stricted geographical distribution. The majority of

America, including Mexico.
With the noteworthy ex-

most species of Trisetum have a rather re-

—

the species are from Mexico, where 9 are endemic,
and only J. irazuense (Kuntze) Hitche. extends from
Mexico and Central America to Ecuador in South
America.

The systematic relationships of the Mexican and
Central American species of Trisetum are not well
known, in part due to the close affinity with Pey-
rischia E. Fourn. and Sphenopholis Scribn. Four-
nier (1886)
one species from Mexico and Guatemala, P koele-
Fourn. Hitchcock (1939) also rec-
his treatment of the North

described the genus Peyritschia with

rioides (Peyr.) E.
ognized Peyritschia
American flora. Koch (1979) transferred to Peyrits-
chia a second species from Mexico, Costa Rica, and
Seribn. [= Р.

Hernández-Torres

Guatemala, Deschampsia pringlei
pringlei (Scribn.) S. D.
and Koch (1987) did not recognize Peyritschia and

Koch].

placed both of these species in Trisetum. The sys-
tematic position of these two species Trisetum
has not gained universal acceptance, although some
recent treatments recognize Peyritschia (Clayton &

Renvoize, 1986: Watson & Dallwitz, 1992; Finot.
2003a). One further species, Peyritschia conferta
Pilg.) Finot, occurs in Venezuela, Ecuador, and Bo-

—

livia. Peyritschia differs from Trisetum in having 1-
nerved glumes, lemmas with bilobed apices that are
awnless, mucronate, or with a well-developed awn
borne near the base, paleas that are tightly en-
closed by the margins of the lemma, and florets
with only two stamens. Trisetum has a first glume
l- to 3-nerved, a second glume 3- to 5-nerved, lem-
ma apices with 2 to 4 short awns with the central
awn inserted above the middle of the lemma, paleas
that are not tightly enclosed by the lemma (i.e..
gaping), and florets with 3 stamens.

Sphenopholis was described by Scribner (1906)
to include seven species and seven subspecies. He
characterized the genus as having spikelets that
disarticulate below the glumes and between the flo-
rets, second glumes that are usually broadly ob-
ovate, and lemmas with an entire or 2-toothed apex
that is awnless or awned just below the apex. In
contrast, Trisetum has spikelets that disarticulate
above the glumes and between the florets, second
glumes that are lanceolate to ovate, and lemmas
with a biaristulate to bidentate apex that is awned
on the upper third. On the basis of these characters,
Scribner (1906) transferred three species of Trise-
tum to the new genus Sphenopholis: S. interrupta
(Buckley) Seribn.. S. hallii (Scribn.) Seribn.. and S.
palustris. (Michx.) Scribn. Hitchcock (1939) and
Hitchcock and Chase (1951) retained these three
species in Trisetum, although Hitchcock (1915) ear-
lier placed S. palustris as a synonym of a fourth
species, S. pensylvanica (L) Hitche. Erdman (1965)
also recognized S. pensylvanica but did not include
5. interrupta, although he recognized that this spe-
cies resembles Sphenopholis in spikelet disarticu-
lation.

Volume 91, Number 1

Finot et al. 3
8 5 Peyritschia & Sphenopholis

Steudel (1854).

made one of the earliest enumerations of Trisetum

who recognized four species.

"p

in Mexico: T. deyeuxioides (Kunth) Kunth, T. elon-
gatum (Kunth) Kunth, T. tolucense (Kunth) Kunth,
and T. viride (Kunth) Kunth. An important contri-
bution to the knowledge of Mexican species was
made by Fournier (1886). who described six new
species: T. gracile E. Fourn., T. nivosum E. Fourn.,
T. interruptum E. Fourn., T. paniculatum E. Fourn..
T. bambusiforme E. Fourn.. and T. virletii E. Fourn.
On the basis of Pringle's collections from Mexico.
(1896) Grasses of North America
T. deyeuxioides var. pu-

Scribner in Beal's
described three new taxa:
bescens Scribn. ex Beal, T. filifolium Scribn. ex Beal
var. filifolium, and T. filifolium var.
Scribn. ex Beal. In a general synopsis of Mexican
Hitchcock (1913) described J. palmeri

Hitche. and mentioned nine other species. By the

aristatum
grasses,

middle of the 20th century, most Mexican species
of Trisetum had been described. More recently.
Morden and Valdés-Reyna (1983) described a new
species, Т! curvisetum Morden & Valdés-Reyna, en-
demic to Nuevo León, Mexico.

Hernández-Torres and Koch (1988) have pub-
lished the most recent revisionary study for all
Mexican species of Trisetum, and they recognized
11 species: T. altijugum (E. Fourn.) Scribn.. T. cur-
T. interrup-
Lum, Torres, T
pringlei, T. spicatum, T. viride, and T. virletu. Es-

0

visetum, T. deyeuxioides, T. filifolium,

T. irazuense, T. kochianum Hern.
pejo-Serna et al. (2000). as a part of the. floristic
list of
southern Mexico the presence of T. angustum Swa-

Mexican monocotyledons, mentioned for
Hen and J. pinetorum Swallen, both originally de-
scribed from Guatemala. Other recent treatments of
the genus are those of McVaugh (1983) for Nueva
Galicia, Herrera-Arrieta (2001) for Durango, and
Herrera and Rzedowski (2001) for Valle de Mexico.

In Central America, Pohl (1980) in Flora Cos-
taricensis mentioned four species: Trisetum deyeu-
xioides. found also from Mexico to Central and
South America, 7! irazuense, T. pringlei from Mex-
ico to Central America, and J. tonduzii Hitche.
known only from Costa Rica and Panama. Mc Vaugh
(1983) and Hernández-Torres and Koch (1988) cit-
ed T. viride from Guatemala. and Herndndez- Torres
and Koch (1988) cited J. kochianum from Guate-
mala and Costa Rica.

The only subgeneric treatment of Trisetum in the
Americas was done by Louis-Marie (1928—1920),
who prepared a key to the subgenera, sections, and
subsections. His Trisetum subg. Heterolytrum Lou-
is-Marie sect. Anaulacoa Louis-Marie included: T.
filifolium, T. interruptum (as T. disjunctum Louis-
T. rosei Scribn. & Merr., T.

Marie), T. irazuense,

spicatum, T. viride (as T. paniculatum E. Fourn.),
and T. virletii. In subsection Sphenophoidea Louis-
Marie he placed Sphenopholis interrupta (as T. in-
terruptum); in subsection Deschampsioidea Louis-
Marie he placed J. palmeri; in subsection
Graphephorum (Desv.) Louis-Marie he placed Pey-
rischia. koelerioides [as T. altyugum (E. Fourn.)

Scribn.. and J. pringlei; in subgenus /solytrum

ouis-Marie he placed Peyritschia deyeuxioides
Kunth) Finot (as

Here. we describe and illustrate four new Mex-

—

Т. deyeuxioides) and T. viride.

ican species of Trisetum (T. durangense Finot & P.
M. Peterson, T. martha-gonzaleziae Р. M. Peterson
& Finot, T. spellenbergii Soreng, Finot & P. M. Pe-
terson, and T. ligulatum Finot & Zuloaga). and we
discuss the systematics for Trisetum, Peyritschia,
and Sphenopholis in Mexico and Central America.
We also include a subgeneric classification of the
species in Trisetum for Mexico and Central Amer-
ica.

MATERIAL AND METHODS

This study is based on the examination of her-
barium specimens from BAA, BAF, C. CHDIR,
CONC, CR. P. QCA, US, S, SI. including the type
specimens of most of the species studied. For an-
atomical observations, hand cross sections. were
made from the central portion of the blade below
the flag leaf; and surface features were observed on
the adaxial portion of the ligule. Abaxial epidermis
preparations were made according to the method in
Metcalfe (1960). Slides were observed on a Zeiss
microscope at SL.

KEY FOR DISTINGUISHING TRISETUM, SPHENOPHOLIS, AND

PEYRITSCHIA

la. Stamens 2: ше s linear, oe | -nerved:
lemmas awnless or awned with a 2-lobate apex:
palea tightly enc idee by ilie margins of the lem-
ma (not gaping) Peyritschia

Ib. Stamens 3: glumes
or oblance Р li e first glume I- to

-nerved; lemmas
or entire or

^s lanc solate. OV ate-lanccolate.

3-nery mer second glume 3- to
with 2 to 4 short awns at the ap
2-toothed: ds a not tightly enc lused by the mar-
gins of the lemma (gaping).

Perennials: disartic anaes between the flo-

rets and above the glumes: upper glumes

lanceolate to ov sue ырга n Trisetum

3a. Lemma apex opaque, the intermediate

1

s; awn inserted on the upper
third of the lemma

y

я isetum subg. Тешип
ш ТЕ le lax, + open, ovate to py-
ramidal Trisetum sect. Trisetum
4b. Panicle narrow, spic iform —
Trisetum sect. ма

Annals of the

4
Missouri Botanical Garden

3b. Lemma apex hyaline, without nerves or Avena joi ie Kunth, Nov. Gen. Sp. 1: 148 1616, Tri-
with both intermediate and marginal um elongatum (Kunth) Poir., Басус), 366.

nerves extended beyond the apex as 817. Trisetum ee (Kunth) Kunth, Rev.

four short awns; awn inserted on the an 1: 101. 1829. TYPE: Mexico. In scopulosis

middle of the lemma prope urbem "hus 1833, aoe s.n. (holotype,

risetum subg. Desc жое P!; isotype, US-3102206
2b. Annuals or perennials; disarticulation of flo- Calamagrostis н Buc tes. Pre lim. Rep. Surv.
rets below the glumes: upper glumes oblar Texas 2. TYPE: U.S.A. Texas. [No type ma-
ceolate to obovate Sphenspialis terial has bee sn loc rated, ak the type locality is
presumed to be Texas, Buckley did not cite a loc ality
TAXONOMIC. TREATMENTS n is did i mention a collector in his original pro-
olog
Sphenopholis Scribn., Rhodora 8: 142. 1906. Т kalli Se ‚ Bull. Torrey Bot. Club 11: 6, 1884.

TYPE: Sphenopholis obtusata (Michx.) Scribn.

Annuals or perennials, without rhizomes: culms
20-120 cm tall, glabrous.
sparsely pubescent; ligule membranous; blades 1—

«al sheaths glabrous or

12 mm wide, glabrous or sparsely pubescent, flat,
soft. Inflorescence in panicles 5—25 cm long, lax
3-flowered; pedicels
the

glumes; glumes heteromorphic, usually shorter than

and narrow. Spikelets 2-

short and glabrous: disarticulation below

the spikelet; first glume narrow, shorter than or as
long as the second glume, linear-lanceolate, l-
nerved; second glume obovate to oblanceolate, 3-
to 5-nerved: lemmas smooth or scabrous, muticous
or awned, 3- to 5-nerved, blunt to biaristate at the
apex; awn, when present, borne on the upper third
of the lemma: callus glabrous to subglabrous; palea
2-keeled, shorter than its lemma; lodicules 2, mem-
branous, minutely dentate at the apex, 0.5 mm
long; stamens 3, anthers 0.5-1 mm long: ovary gla-
brous. Caryopsis with liquid endosperm.
Sphenopholis is a small genus with five species
from Canada to Mexico (Clayton & Renvoize.
1986). Erdman (1965) revised Sphenopholis and
recognized four species in addition to the hybrid
Sphenopholis Xpallens (Bichler) Seribn. [S. obtu-
Scribn. X S.
Two species are represented i

pensylvanica | (L.)
Mexico

sata (Michx.)
Hitche. |.
and Central America.
KEY TO THE SPECIES OF SPHENOPHOLIS IN MEXICO. AND
CENTRAL AMERICA
la. Lemmas awned, the awns 4—8 mm long: spike-
lets 4-6 mm long 5. interrupta

Ib. Lemmas unawned: spikelets 1. 5-3.6 mm n
2. S. obtusata

la. Sphenopholis interrupta (Buckley) Scribn.
subsp. interrupta, Rhodora 8: 145. 1906. Ba-
sionym: Trisetum interruptum Buckley, Proc.
Acad. Nat. Sci. Philadelphia 14: 100. 1862.
TYPE: U.S.A. Middle Texas, Buckley s.n. (lec-
totype, designated by Hitchcock (1935: 973),
PH not seen.; isotype, US-fragment & photo ex

PH!).

ribn
Senha hallii (Scribn.) Seribn.. pee 8(92):
1 46. ›. Fisetum inte و میا‎ | NR ED hallii
(5с ib n. a Нисһе. TYPE: U.S 5 prairies
Houston, 1872, Hall 799 Ыы US-72664!).

Annual; culms 10—40 em tall, glabrous, mostly
3 nodes, the nodes glabrous. Leaf sheaths glabrous
or sparsely pubescent, with one side extended up-
ward, shorter than internodes; ligules 1 mm long,
truncate, ciliate,
blades 3-10 em X 1—4 mm, flat. Panicles 5-12 em
X 4-15 mm, narrow. Spikelets 4-6 mm long, 2- or

pilose on the dorsal surface:

3-flowered: rachilla sparsely pubescent; glumes
3.5-5 mm long, about equal in length and equaling
or shorter than the spikelet, glabrous, scaberulous
along the keel; first. glume linear-lanceolate, 3-
nerved; second glume obovate to oblanceolate, 5-
nerved; lemmas 3.5-5 mm long. lanceolate. gla-
brous, 3- to 5-nerved, 2-aristulate at the apex,
awned on the upper third of the lemma: awn 4-8
mm long, slightly twisted and twice geniculate; pa-

ea 2-2.5 mm long. about half the length of the

lemma, 2-nerved, the nerves scabrous, 2-dentate at
the apex: callus glabrous to subglabrous; lodicules
0.5 mm long, slightly bilobate at the apex, the lobes
Anthers about 0.5 mm

rounded, obtuse to acute.

long.

Distribution. U.S.A. and Mexico. According to
Gould and Moran (1981), Sphenopholis interrupta is
the southwestern United

widely distributed in

States.
MEXICO. Baja California: near
1 Apr. 1886,

Specimens studied.
U.S. Boundary, “Northern Lower California."
C. R. Orcutt 1431 (US).

KEY TO THE SUBSPECIES OF SPHENOPHOLIS INTERRUPTA
S. interrupta subsp. interrupta

la. Glumes glabrous ^
5. interrupta subsp. californica

Ib. Glumes pubescent

Ib. Sphenopholis interrupta subsp. californi-
ca (Vasey) Scribn., Rhodora 8: 146. 1906. Ba-
sionym: Trisetum californicum Vasey, U.S. D. A.
Div. Bot. Bull. 13(1): t. 46. 1892. Trisetum in-
terruptum Buckley var. californicum (Vasey)
Louis-Marie, Rhodora 30: 240. 1929, TYPE:

Volume 91, Number 1
2004

Finot et al.
11 5 Peyritschia & Sphenopholis

Mexico. Northern Lower California, C. К. Or-
cutt 1437 (lectotype. designated by Hitchcock
(1939: 552) and Hernández-Torres & Koch
(1988: 80), US-868402!; MO-
2526390 not seen).

isotype.

Glumes pubescent, the trichomes 0.1—0.4 mm
long.

Distribution.
lifornica was described for Northern Lower Califor-

Sphenopholis interrupta subsp. ca-

nia, and its distribution seems to be restricted to
the type locality.

Notes. Hitchcock (1939) designated the lecto-
type for Trisetum californicum without explicitly cit-
ing the herbarium. Hernández-Torres and Koch
(1988) then specifically designated the US sheet as
the lectotype.

Comments. Though the systematic position of
this taxon in Sphenopholis was proposed by Serib-
ner (1906), subsequent treatments by Louis-Marie
(1928-1929). Hitchcock. and Chase (1951).
Erdman (1965) excluded this species from Sphe-

and

nopholis. According to Erdman (1965) further study
is needed to clarify the generic placement of this
species. On the basis of micromorphological char-
acters of lemma epidermes of several genera in
Aveninae, including Trisetum and typical species of
Sphenopholis, Finot and Matthei (unpublished re-
sults) support the generic position of this species
in Sphenopholis. Louis-Marie (1928-1929) created
Trisetum subsect. Sphenophoidea for species that
disarticulate below the glumes and included in this
T. interruptum, T. interruptum var. californicum, T.
hallii, T. pensylvanicum (L) P. Beauv., T. palustre
(Michx.) Torr..
lieve that all of these species belong in Sphenop-

holis.

and T. ludovicianum Vasey. We be-

N

. Sphenopholis obtusata (Michx.) Seribn., Rho-
dora 8(92): 144. 1906. Basionym: Aira obtu-
sata Michx.. Fl. Bor. Amer. 1: 62. 1803. Ai-
ropsis pid (Michx.) Desv.. J. Bot. appl. 1
200 . Poa шам (Michx.) Link, Hoy:
Berol. 1: E^ Agrostis 1 (Michx.)

Steud., Nomencl. Bot. ed. 2. 1: 41. 1840. Koe-

leria obtusata (Michx.) Trin. ex i» d., No-

mencl. Bot. ed. 2. 1: 41. 1840. Reboulea ob-

tusata (Michx.) A. Gray, Manual 591. 1848.

Eatonia 1 (Michx.) A. Gray, Manual ed.

2, 558. 6. TYPE: U.S.A. Florida: Michaux

s.n. duas pe. designated by Hitchcock (1908:

152), Pl. photo NY not seen & US!

US-72667-fragment!).

; Isotype.

Deser. Gram. 83. 1817. Koeleria

Aira truncata Muhl.,

) Torr. Fl. N. Middle United States
. TYPE: U.S.A. Pennsylvania:
е 127 (holotype, PH not seen; isotype, U Ф
1535792-fragment!).
Koeleria 1 Nutt., Gen. N. Amer. Pl. 2: (Add. 2).
1818. : U.S.A. East Florida. J. Say s.n. (ho-
da PH not seen, photo US!; isotype, US-frag-

truncata er
1: 116.

itt).
канна gracilis з Revis. Gram. 2: 341, t. 84. 1630,
illeg. TYPE: Michaux s.n. (holotype, B not
seen; isotypes, 34 US- 76319- dang ex В!).
Trisetum pts Trin., Mem. Acad. Imp. Sci. St.-Peters-
urg, Ser. 6, Sci PME ]: 66. 1 аорта
obtusata subs lob a (Trin.) Scribn.. Rhodora 8:
144. 1906. ee obtusata var. lobata (Trin.)
Scribn. ex B. L. Rob., Rhodora 10: 65. 1908. TYPE:
Ad flumen dc a (Red River), inna borealis
holotype, LE-TRIN- 2437.01!).

Eatonia density ra E. Fourn.. 1886.

y 11.
1886. nom. inval. TYPE: U.S.A. Texas: Bear Feb.
1839, J. L. Berlandier 1617 (holotype, W not seen:
e S, B not seen, LE-TRIN-1951.02!, US-72668-
fra nt!).

Eatonia pre var. robusta Vasey ex L. H. Dewey, Contr.
U.S. Natl. Herb. 2: 544. 1894. аси гоню (Va-
sey ex L. H. Dewey) Rydb., Bull. v Bot. Club
32: 602. 1905. Sphenopholis robusta em ex L. Н.

. 6: 12. 1910. TYPE:

ille, i Wallis s.n. (holotype,
otype, NY not see

Eatonia pene var. robusta 5 ex Rydb., Contr. U.S.
Nall. Herb. 3(3): 190 5 nom. illeg. hom. TYPE:
U.S.A. Nebraska: Mullen, P. A. Ry a erg 1807 (ho-

зе, not located; 1 NY,

Eatonia obtusata Mo 5 uem ex Rydb. &
Shear. Bull. Div. Agrostol. U.S.D.A. 30. 1897.
е уаг. Mes fo. purpurascens

\ tydb. & Shear) Waterf., Rhodora 50: 93.
19. a TY i TSA Oklahoma:

Palmer 404 (lec m
Bus ock (1935: 956), US-868756!).

Eatonia еи Seribn. & Merr.. n il. Div. Agrostol.
U.S.D.A. 26: 6. 1900. Sphenopholis d subsp.
Mr ear ы ribn. & Merr.) Scribn., Rhodora 8: 144
1906. Sphenopholis obtusata var. une ens (Scribn.
& Merr.) Seribn. ex B. IL. Rob., Rhodora 10: 65.
1908. Sphenopholis 5 (Seribn. & Merr.) A
Heller, Muhlenbergia 6: 12. 1910. Re Boule eres

False Washita,
designated by

var. pubescens (Scribn. & T rr.) Farw.. id ». Michi-
gan Acad. Sci. 17: 181. 1916. TYPE: n
sissippi: Starkeville, 30 Apr. 1891, 5. i "Tay s.n.

(holotype, US-72070!).

W. Amer. Sei. 15: 50. 1906. Sphe-

nopholis е (Suksd.) A. Heller, а Ө:
910. TYPE: U.S.A. Oregon: n Jalles

on iiw River, 8 June 1897, r^ pese

1553 (isotypes. F not seen, GH not seen, ISC not

NY not seen, UC not seen, US-72

т annua Suksd.,

seen,

Annual: culms 20-120 em tall. Leaf sheaths gla-
brous, scabrous. or finely pubescent: blades 8-15
cm X 3-12 mm, flat. Panicles 5-25 cm X 5-20
mm, narrow. Spikelets 1.5-3.6 mm long, 2- or 3-
flowered: rachilla mostly glabrous; glumes 1—3(-
3.6) mm long. about equal in length, dimorphic,

Annals of the
Missouri Botanical Garden

shorter than the spikelet, scaberulous especially
along the keel: first. glume linear-lanceolate, 1-
nerved; second glume conspicuously obovate, 3-
nerved; lemmas 1.8-2.8 mm long, lanceolate. gla-
brous to scaberulous, entire at the apex. unawned:
callus glabrous; anthers 0.5—0.7 mm long.

Anatomy and micromorphology. ligule apices
with papillose cells and short, stiff trichomes; ligule
epidermis composed of long cells with straight
walls; stomata absent; macrohairs absent; prickles
present. Foliar epidermis with long cells rectan-
gular to fusiform, with sinuate lateral walls: short
cells present in costal zones only, rectangular, with

sinuous walls: trichomes absent; stomata present.
MEXICO. ¢ Diaz,

Specimens studied. Coahuila:

Grande V Valley,

е Hitchcock 5893. Di urango: city ar D u-
rango & vicinity, June li 890. : digi 255 (US).

0 (US) Nuevo. León: Tiere rev, re vis

ALS. ‘cd 5571 ‚ Oaxaca: Oaxaca . 12, 1 ug.
1910, LU pos (US). Puebla: Fane E E
.20 ud . Nicolas s.n. (US); С.

ae s.n. (US).
577 (US

1890, V. Palmer

denda d

Mexic. Pl. 2:

koelerioides

109. 1880.
(Peyr. E.

Peyritschia E. Fourn.,
TYPE:

Fourn.

Peyritschia

Perennials, with or without rhizomes; culms 20—
200 cm tall, mostly glabrous. Leaf sheaths glabrous
or pubescent: blades flat: ligule membranous. Inflo-
rescence in panicles narrow, contracted, spiciform
or lax and somewhat open. Spikelets 2-flowered:
rachilla glabrous to copiously pubescent: disartic-
ulation above the glumes and between the florets:
glumes isomorphic, 1-nerved, equal or subequal. as
long as the spikelet or longer: lemmas bilobed at
the apex, awned near the base or the middle of the
lemma, rarely muticous or shortly mucronate near
the tip (P. koelerioides mucronate or muticous): pa-
lea tightly enclosed by the margins of the lemma

(not gaping), 2-keeled; stamens 2; lodicules 2.
membranous; ovary glabrous. Caryopses with liquid
endosperm.

KEY TO THE е OF PEYRITSCHIA IN MEXICO AND
CENTRAL AMER

|

а. Lemma without а 17 awn, apex muticous o1
with a subapical тист 2. P. koelerioides

Lemma with a dorsal awn, borne near the middle

or upper third of the lemma, the awn geniculate

and extended beyond the glumes.

—

2a. Rachilla copiously pubescent, ER trio homes
lor

2-3 mm long deyeuxioides

2a. s pubescent, the trichomes only 0.2—
0.8 mm long.
3a. C ulm is 5-12 cm tall: leaf blades 2.5-3.5
em long: panicles about 2.5 em long,
0.5 em wide, contracted, narrow
P. humilis
le af lade 8 5-

w

C ulms 20—200 em tall;

poni narrow but 1 ‘ly

open P. pringlei
l. Peyritschia deyeuxioides (Kunth) Finot.
Contr. U.S. Natl. Herb. 48: 478. 2003. Ba-

sionym: Avena deyeuxioides Kunth, Nov. Gen.

Sp. 1: 147. 1816. e E
(Kunth) Poir., Encycl. Suppl. 5: 366. 1817.
Trisetum deyeuxioides (Kunt и Kinik. Rev.
Gram. 1: 102. 1829. i a triflora Nees,
Linnaea 19: 691. 1847. : Mexico. "Ad

| отой & Воп-
pland s.n. (holotype, PI; isotypes, BM not seen,
LE-PRIN-1913.05!, US-865589 fragment. ex

PD.

ripam. Lacus Tezcucensis,’

Avena tric hopodia J. Presl, Reliq. Haenk. 1: 254. 1830.
TYPE: Mexico. Haenke s.n. (hok otype, PR not seen;
T E-TRIN-1945.01a!, US-0865583 frag-

ment ex Ad
sa evoluta | К. Fo Bull. . Bot. France 24:
81. 18 Trisetum popu. (. i Hitchc.,
С U. s. “Кай, Herb. 17: 325. 1913 РЕ: Mex-
‚ Veracruz: Mirador, 1841, КОМ. тк 730

(le 'clobtype, абаке d by Hitchcock (1939: 557) and
Hernández-Torres & Koch (1988: 78), US-207459!:
isolypes, C not. seen, LE! MO-3056872!. P not
seen).
Trisetum var. Beal,
d

pr Scribn. ex
Gras Ў e 374. . TYPE: Mexico.
dn acán: dry hills near diei 'uaro, 19 Nov. 1891,
G. Pringle 3950 а MSC not seen; isot
H not seen, 3 not seen, МЕХ
3050871 not seen, P!, US-868407!).

Bs ^yeuxioides
5 М. А!

"у pes,

MO-

2:

nol seen,

Perennial, without rhizomes: culms 50-180 cm
tall, glabrous. Leaf sheaths glabrous or pubescent;
ligule 1—3(—5) mm long, truncate, erose, glabrous:
blades 0.54 mm wide. flat, narrow toward apex,
glabrous or sparsely pubescent, sometimes densely
pubescent. Panicles 10-35

1-5 ст, lax, some-
what open and nodding. Spikelets 4.5-8 mm long,
2- or 3-flowered: rachilla copiously pubescent, the
trichomes 2-3 mm long; glumes (3.5-)4-5.5(-8)
mm long, equal, shorter or longer than the florets,
linear; first glume with a green midnerve, purplish
otherwise, the margins usually hyaline, the keel
scabrous; lemmas 4-6 mm long. glabrous, terete,
rounded in cross section, 5-nerved, nerves incon-
spicuous, dorsally awned near the middle or upper
third of the lemma: apex entire, bilobed or biden-
tale: 4.5-8(-12) mm long. geniculate and
twisted, purple, scabrous; callus short. pubescent,

awn

Volume 91, Number 1
2004

Finot et al. 7
1 8 a Peyritschia & Sphenopholis

the trichomes 0.3-1 mm long: paleas 2.5-3.5 mm
long; lodicules 0.5 mm long, linear, narrow, irreg-
ularly lobed at the apex: anthers 1.3-1.7 mm long.

Caryopses 1.8-2.5 mm long.

Chromosome number. 2n = 14, 28 (Tateoka,
1962: Hernández-Torres & Koch, 1988).
Anatomy. Leaf blades are slightly keeled in
transverse section, abaxial ribs not well developed.
furrows less than one half of the leaf thickness:
vascular bundles of first and second order with ad-
axial and abaxial girders, bundles of third order
with adaxial and abaxial strands; marginal scleren-
chyma present; bulliform cells large, conspicuous,
in fan-shaped groups at the base of adaxial furrows:
abaxial epidermis with long rectangular to fusiform
intercostal cells; costal zone with cork cells and
silica bodies in short rows or more rarely in cork
cell-silica body pairs; prickles present.
Distribution.
Costa Rica, El
Mexico (Aguascalientes, Chiapas, Chihuahua, Dis-

Mexico to Ecuador Colombia.
Salvador, Guatemala, Honduras.
trito Federal. Durango, Guerrero, Guanajuato, Hi-
dalgo, Jalisco, México, Michoacan, Morelos, Oaxa-
ca, Puebla, Veracruz.
Zacatecas). Nicaragua, Panama, Venezuela | (Pohl &
Davidse, 1994: Finot, 2003a) in humid prairies and
open woods, 1000—2000 m.

Notes. Hitchcock (1939) designated the lecto-
type for Deyeuxia evoluta without explicitly citing
the herbarium. Hernández-Torres and Koch (1988)
then specifically designated the US sheet as the
lectotype

Queretaro, San Luis Potosí,

Comments. Based on 25 morphological char-
acters, Koch (1979) pointed out that P. deyeuxioides
shows an intermediate position between Peyritschia
and Trisetum. However, the androecium is com-
posed of only two stamens, the glumes are l-
nerved, the lemma is terete and dorsally awned
near the middle, the apex of the lemma is bilobed,
and the palea is tightly enclosed by the margins of
the lemma. These characters indicate that this spe-
cies should be placed in Peyritschia.

Specimens studied. COSTA RICA. Cartago: Cordil-
lera Central, Volcán Irazú. 2 km NW к, reg: 19
Nov. 1968. Pohl & Davidse 11449 (CR). MEXICO. Chi-
huahua: 19.6 km W of Balleza & 74.2 km E и Guacho-
chi, 18 Sep. 1991, Peterson et al. 10752 (US); 24.2 km 5
of San Juanito & 4.8 km N of € d on MEX 127, 10 Sep.
1989. P eterson et al. 8007 (US); 122.5 km W of La Junta
d y зк hic in (ame Nacional Cascada
. 1989, Peterson & King 8231 (US);
of = 200. 13 Oct. 1887, Pringle 1432
(US); Sierra Madre Oc c ide p Parque Natural 1 a

del Cobre, 13.6 mi. 1 Bufa on road toward 5
31 Oct. 1995, 9 ор el al. 13575 (US 3. (os:
иша: Sierra Madre Oriental, 5 mi. W of Chapultepec on

—

canyons

2 Nee

cutoff road between Hwy. 54 & 57, 23 mi. S of Saltillo,
16 Oct. 1995, Peterson & Knowles 13276 (US); ca. 5 km
Е of Salltillo (Las Palapas) up camino de Quatro, 20 Sep.
2003. Peterson et al. 17868 (CIIDIR, US). Distrito Fed-
eral: Desierto de Los Leones, 19 Oct. pi Tateoka 1152
(US). кош 2 km of San Miguel de La Michilia. 24
Sep. 1991. Powis et al. 10913 (US); 16.1 km NW of
MEX 40 on logging road to Santo Domingo, 5 Oct. 1989,
Peterson & King 8288 (US); 20 mi. SE of ео on
road to Charcos, 7 Nov. 1995, Peterson et al. 136.
Hida mat bogey us of Lago 2 a below ш
24 July 1947, Moore Jr. 3466 ). México: Valle
de Mexico, 10 үте 1901, Pringle 051 (P). Shaffner 15
(P); prope Tacubaya, Shaffner 319 (P). Michoacán: 15.5
km SE of Zacapu on MEX 15 km toward Quiroga. | Oct.
1991. Peterson et al. 10994 (US). Morelia: San Miguel,
8 Aug. 1912, Arsénes 8645 (P). Oaxaca: on weep Road
19 km from Ti . 1963, McKee 10869 (P).
Querétaro: 16 mi. E of Landa, 12 Dec. 1900, Smee
& Johnston s.n. (US). San Luis Potosi: between Puerta
Huerta and Rioverde in the Sierra de Alvarez, IT Sep.
1954. Sohns 1177 (US); near Puerta Huerta in the Sierra
de Alvarez. 4 Sep. 1954, Sohns 1034 (US).
2. Peyritschia koelerioides (Peyr.) E.
Mexic. Pl. 2: 1886. Aira koelerioides
Linnaea 30: 5. 1859. Deschampsia koe-
lerioides (Peyr.) Benth., J. Linn. Soc., Bot. 19:
96. 1881. TYPE: Mexico. México: Volcan de
Toluca. 8800 ft., 1846, C. Heller 311 (holo-
type. P not seen; isotype, US-1647945-frag-
ment ex P-DRAKE)).

Fourn.,

Peyr.,

Е . E. Fourn., Mexic. Pl. 2: 111.
1886. tum. altijugum Е. Tourn. | pg
dora 8/89): 89. 1906. TYPE: Mex

SJ
8

xico. Veracruz: in
monte Orizabensi, 5 ft. T. M. Lieb-
not seen; isotype, US-

mann 603 (holotype, P
5!).

culms 25-85 cm
tall, glabrous; nodes 2 or 3, glabrous. Leaf sheaths
glabrous, rarely pubescent, shorter than the inter-
nodes; ligule 1-3 mm long, truncate, erose; blades
1.5-4 mm wide, usually glabrous, flat. Panicles 7—
20 cm X 4-8(-10) mm, spiciform: rachis and ped-
icels scabrous. Spikelets 3-5 mm long. 2-flowered:

Perennial, rhizomes absent:

rachilla glabrous to sparsely pubescent, the tri-
chomes less than 0.5 mm long; glumes 3—5 mm
long, lanceolate to ovate-lanceolate, equal, longer
than the florets, 1-nerved; lemmas 2.5—4 mm long.
glabrous, terete, dorsally rounded, 5-nerved; apex
унет the lobes short, obtuse, muticous or with
a mucro about 1 mm long or less borne near the
apex: callus glabrous or short pubescent, trichomes
less than 0.5 mm long; paleas 2.4-3.8 mm long:
anthers 0.5-1.3 mm long. Caryopses 1.5-3.5 mm
long.

Chromosome number. 2n = 28 (Tateoka, 1962:

Hernández-Torres & Koch, 1988).

Annals of the
Missouri Botanical Garden

Micromorphology. — Ligule apices have papillate
cells and short trichomes, the epidermis with more
or less rectangular long cells, hooks, and trichomes:
no stomata were seen,

Distribution, Southern Mexico (México, Mi-
choacán, Oaxaca, Veracruz) and Guatemala (Pohl
& Davidse, 1994; Finot, 2003a). 2400-4300 m.

‚решили studied. MEXICO. México: 20 km al NE
Texcoco, sobre la carretera a ME 10 Oct
1965. Rzedowski 21417 (US); Sic | Oct.
1892, Pringle 4306 (U М); Amecamec a, carretera al Paso
de Cortés, 20 a la carretera a
a 18 Oct. 1970,
S of Patzcuaro, 20-25
King & Soderstrom 5159 (US); 20 km NE de
pt 0. sobre la carretera a С alpulalpán. no date, Rze-
dowski s.n. ). Oaxaca: Sierra de San Felipe. Aug.
1894, Pringle 477 75 (P). Puebla: San Nicolás de los Ran-
chos, declive E del Paso de Cortes, 3.5 km NE entronque
de carretera a Amecameca y camino entre Popoc atepetl e

ra Las Cruces,

м 90 Eus ESE de Amecameca, 3 1976,

Koch 73309

3. Peyritschia humilis (Louis-Marie) Finot.
Contr. U.S. Natl. Herb. 478. 2003. Ba-

sionym: Trisetum humile Louis-Marie, Rhodora

30: 244. 1929. Deveuxia gracilis E. Fourn..
Mexic. Pl. 2: 106. 1886, nom. illeg.. non De-

yeuxta gracilis Wedd. 1875. TYPE: Mexico.
Mirador, К M. Liebmann 602 (holotype. Cl:
isotypes, US-3048345
Haun.!).

fragment ex hb.

Perennial: culms 5—12 cm tall. Leaf sheaths flat-
tened; ligule membranous. short, laciniate: blades
2.5-3.5 cm long. Panicles 2.5 X 0.5 em. contract-
ed, narrow, exserted. Spikelets 4 mm long, 2-flow-
ered; pedicels glabrous; rachilla 0.5 mm long. pi-
lose, the trichomes less than 0.8 mm long: glumes
і mm long, equal, lanceolate, longer than the
spikelet, slightly scabrous on the keel, acute at the
apex: lemmas 3-3.5 mm long, terete, awned. the
margins involute toward the base, bilobed at the
apex, the lobes obtuse: awn 4—5 mm long, inserted
from the middle to the lower third on the dorsal
twisted and callus obtuse,

surface, geniculate:

sparsely pilose, trichomes ca. 0.2 mm long: paleas
shorter than the lemma and enclosed by the mar-
gins of the lemma. Caryopses ca. 2 mm long.

Comments. The type of Deyeuxia gracilis E.
Fourn. conserved in Copenhagen (C) includes a

complete plant, 12 cm tall, and a fragment of the
panicle, identified by Hitehcock and Chase as Tri-
Richt.

identification.

setum spicatum (L.) K. The isotype in US

bears the Hernández-Torres

and Koch

within J. spicatum., followed this criterion. The mor-

same

(1988). who synonymized the species

phology of the spikelets confirms its placement
within Peyritschia: spikelets 4 mm long, 2-flowered:
glumes equal, l-nerved, longer than the spikelet;
lemma with a bilobed apex, the awn geniculate and
twisted, inserted near the middle of the lemma: cal-
lus with short trichomes; rachilla sparsely pilose;
stamens 2; ovary glabrous.

Trisetum humile Louis-Marie was a new name for
the illegitimate Deyeuxia gracilis E. Fourn. 1886.
non Weddel 1875, and therefore we use it as the
basionym for the new combination in Peyritschia.

4. Peyritschia pringlei (Scribn.) S. D. Koch, Tax-
on 28: 233. 1979. Basionym: Deschampsia
pringlei Scribn., Proc. Acad. Nat. Sci. Phila-
delphia 43: 300. 1891. Trisetum kochianum
Hern. Phytologia 61: 4. 1987
TYPE: Mexico. Chihuahua: wet places, pine
plains, base of Sierra Madre, 7 Oct. 1987, C.
G. Pringle 1429 (holotype, US-747292!; iso-
types, LL not seen, MEXU not seen, MICH not
seen, US-867629!, US-821538!. VT not seen).

Torres,

Perennial, without rhizomes; culms 20-200 em
tall. Leaf sheaths glabrous, rarely pubescent: ligule
0.5—4 mm long, truncate or rounded at the apex;
5-20
X 1-34) em, narrow but relatively open. Spike-

blades 5-15 em X 1.5-4 mm, flat. Panicles
lets 4-5.5 mm long, 2- or 3-flowered: rachilla pu-
bescent, the trichomes 0.2-0.8 mm long: glumes 4—
5.3 mm long, lanceolate, as long as the florets or
longer. apex acute: lemmas 3-4.3 mm long, gla-
brous, terete, bilobed at the apex. rounded in cross
section, awned near the base; awn 4.5-7 mm long,
geniculate and twisted, exserted: palea 2.3-3 mm
long, shorter than its lemma; anthers 0.8-1 mm
long. Caryopses 1.5-1.7 mm long. fusiform- cylin-
drie.

Inatomy and micromorphology. Ligule apices
composed only of papillate cells, epidermal long
cells rectangular to fusiform, with few hooks and
no trichomes: no stomata were seen. Leaf blades in
transverse section without a keel, without well-de-
veloped ribs, furrows less than one half of the leaf
thickness: all vascular bundles, except the marginal
ones, with both adaxial and abaxial girders; mar-
ginal sclerenchyma absent; abaxial epidermis with
rectangular long cells with straight side walls. cos-
tal cork cells and silica bodies present. prickle
hairs present.

Distribution. Mexico (Aguascalientes, Chihua-
hua, Chiapas, Durango, Guanajuato, Hidalgo, Jalis-
San Luis Potosí. So-
Rica,

Venezuela, Ecuador (Espejo-Serna et al., 2000: Fi-

». México, Puebla, Querétaro.

nora, Tlaxacala). Guatemala. Costa

Volume 91, Number 1
2004

Finot et al.
sven Peyritschia & Sphenopholis

not, 2003a). The documentation of the presence of
this species in Venezuela and Ecuador provides
new records for the distribution of Peyritschia prin-
glei. It was collected by Peterson & Judziewicz
9302, in the Provincia de Bolivar, ca. 3000 m, in

the Andes of Ecuador, and by Peterson & Judzie-

wicz 9477 in Provincia de Loja, Ecuador. Lasser
found the species in Mérida, Venezuela. in 1942
(Lasser 431).
Koch (1988) this species also occurs in Guatemala.
Elevations range from 1600 to 3270 m.

According to Hernández-Torres and

Specimens studied. COSTA RICA. Cartago: Cordil-
lera Central, lower slopes of Volcán Irazú. 1 km below 4
Juan A р 8 Nov. 1968. а & Davidse 11416 (
ECUADOR. Bolivar: 14.5 5 of Guaranda on ы to
Río es 24 May 1990, us & Judziewicz 9302
(US). Loja: 6 km W of Colaisaca on road to Sozoranga, 2
June 1990, Peterson & Judziewicz 9477 (US). GUATE-
MALA. Quezaltenango: 19 June 1954, Koninck 137
(US). MEXICO. Chihuahua: 85.4 km W of Balleza and
8.8 km E of Guachochi. 19 Sep. 1991, Peterson et al.
10786 (US); 38.6 km SW of La Junta « ca. 70.8 km
of Creel at t Pas so Arroyo Ancho crossing, 24 Sep. 1988,
Peterson & Annable 5848 (US) Miñaca, 13 Oct. 1910,
5). Durango: 45 km W of Durango on
Hwy. 40. toward 5 Salt to. 2 Oct.

`~

PA шын

‚ 1995. Peterson et al. 13679 (US); 24 mi. NE of El
Salto on Mani 40 ud Durango. a Oct. 1995, Peterson
et al. 13471 (US); W of Ciudad Durango, У mi. W of E
Salto, s Aug. 19: 58. Reeder & Reeder 3124 (US): 4 mi.
E of El Salto, 1 Oct. 1953, ке « кы: 2561 (US):
20 mi. S of Mezquital. 11 Sep. 2
chez-Alvarado 17729 (CHDIR. 5
M e San Felipe. 27 Oct. ТА Sohn 0 (US). Hidal-
go: Pachuca. 6-7 Sep. 1910, Hitchcock бт 30 (US): Hitch-
cock 6737 (US). Jalisco: Sierra Cacoma. Y mi. NW of Los
Volcanes on road toward Mascota. 15 Nov. 1995, Peterson
13724 (US); Tepatitlán-Guadalajara, 26 Sen, 1946. Her-
nández X., Ruppert & Guevara 2694 (US); Zempoala, 15
km N of Ciudad Sahagán & 1 km NE of л -mpoala, sobre
la carretera a Sta. Maria Tecajete. 26 Aug. 1977. Koch
77179 (US); Mineral del Chico, Parque Natural El Chico,
17 km al N de la carretera Pac 'huca-Zac xL 4 Dec.
: Toluca. 13 5 1910,

1 Marcos. sien em-

977. Koch 77532 (US
Нисћсос i 6889 (US).
bankment, 29 Aug.

El к. А 10 km al E de ye 19?09' N,

. Tenorio 15165 (US). Querétaro:
erro Zamorano, Min: с Pa 13 Nov. 1971. Rze-
dowski & ` MeVaugh 473 (US). = Luis Pavia: 15-18
July 1910, Hitchcock 5685 (US): Cañón del Lobo, Sierra
de San Miguelito, Sohns 1/62 үа Puerta Huerta i in the

1 Sep. 1954. Sohns 1019 (US
cala: ca. ‚ NE of Tlaxco. 23 Sep. 1953. Sohns 597
(US). VENEZUEL A. pa m Banda. near Mérida.
22 Sep. 1942, Lasser 431 (

i mas

Sierra de Alvarez,

m Pers.. Pl. 1: 97. 1805. Trisetarium
Poir, Encycl. Suppl. 5: 365. 1817. nom. su-

perfl. Acrospelion Besser ex Schult. & Schult.

f.. Syst. Veg. Mant. 3: 526, 1827. nom. illeg.
superfl. Rebentischia Opiz, Lotos 4: 104. 1854,

non P. A. Karsten 1869. TYPE:
Ess.

Syn.

nom. superfl.,
Trisetum rd (L.) P. m à

togr. 88, 153, t. 18. f. 1.

Agros-

Rupestrina Prov., Fl. Canad.: 689. 1862. TYPE: Rupestri-
na pubescens Prov. [= Trisetum spicatum (L.) Richt.]

Perennials, caespitose, sometimes shortly rhizo-
matous; culms 5-300 cm tall, erect to geniculate
at base. glabrous or pubescent. Leaf sheaths gla-
brous or pubescent, longer or shorter than the in-
ternodes; blades flat, conduplicate. convolute or in-
soft,
Inflorescence in panicles contracted or open, spi-

volute, rarely rigid; ligule membranous.

ciform, ovate, or pyramidal; the rachis glabrous.
scabrous, or pubescent. Spikelets (1)2- to 6-flow-
ered, short pedicellate: rachilla pubescent or gla-
brous, usually prolonged beyond the upper floret:
disarticulation above the glumes and between the
florets; glumes heteromorphic. lanceolate to ovate-
lanceolate, equal or unequal, first glume l- to 3-
nerved, usually shorter and narrower than the sec-
ond. second glume 3- to 5-nerved: lemmas
lanceolate. (3)5(7)-nerved, usually awned or muti-
cous, with apex and margins hyaline, glabrous or
pubescent, slightly keeled and compressed, rarely
terete: apex with 2 to 4 short awns, entire, or 2-
toothed: central awn from the upper third. rarely
the middle, of the subapical portion of the lemma:
awn exserted, geniculate or merely divaricate: cal-
lus short pilose; palea not tightly enclosed by the
margins of the lemma (gaping). 2-keeled, hyaline.
usually shorter than the lemma: stamens 3, anthers

T

34.5 mm long: lodicules 2, membranous: ovary
ИЕ or with short and shining trichomes near
the apex: endosperm solid or liquid, soft or hard.
Caryopses compressed, soft; hylum short, puncti-

form. Basic chromosome number x = 7.

Our treatment of the

species that occur in Mexico and Central America

Comments. subgeneric

includes two subgenera: Trisetum subg. Trisetum
and 7! subg. Deschampsioidea, and two sections in
subgenus Trisetum: section Trisetum and section
Trisetaera (Appendix 1). In the following key we
have indicated what subgenus and/or section most

species occur in (see leads 5a, Sb, ба, and 8a).

Ккү TO SPECIES OF TRISETUM IN MEXICO AND CENTRAL AMERICA

la. Lemmas with the apex entire, slightly bidentate, or irregularly dentate; nerves of the lemma not prolonged
bevond the apex: lemma muticous or with a short subapical awn (but awned in T. filifolium var. aristatum).

Annals of the
Missouri Botanical Garden

2а. Glumes o ry е in length, shorter than the spikelet, covering nearly half of the spikelet length;
spikelets I- to 3-flowered: lemma with the apex obtuse to irregul: wly dentate; leaf blades flat or some-
times a or involute, never filiform; lodicules lance salate, acute at the apex.

Ja. Panicles 4-12 em wide, open, 5 the branches capillary and flexuous: first glume 1. 42. 6 mm
long: second glume 24.5 mm long T. pringlei

ЗЬ. Panicles 0.6-1 em wide, narrow and densely flowered; the branches с lose ly appre sed; first glume
(2.7—)3—4 mm long: second glume 4—5.8 mm long LE aiam

2b. Glumes 5 10 equal і in length, shoul two-thirds as long as the spikelet or as long as the spikelet
spikelets 2- or 3-flowered: lemma with the apex slightly bidentate to entire; leaf blades involute. filiform:

lodicules line ar, slightly bilobate at the apex.

4a. Lemma muticous or with a short subapical mucro 0.2-0.5 mm long За. T. filifolium var. шш

4b. Lemma awned on the upper third: the awn 3-5 mm long, geniculate
3b. T. Аш ж var. aristatum
Lemmas bidentate at the apex; inte бей. imd — nerves or only intermediate nerves. prolon
beyond the apex as 2 to 4 apical setae; apical teeth some mer wil nerves; lemma aristate, the awn we vell
deve sloped. borne on the upper third, middle, or lower third of the lemma. not 1 5
da. Awn always inserted on the upper third of the lemma (sometimes ne arly in this Prim in J. palmeri);
glumes unequal, the first glume shorter and narrower than the second la apex of the lemma with
two setae formed by the diis ction of the intermediate nerves; lemma + keeled in cross section: palea

е.

gaping (Trisetum subg. Trisetum).
6a. Panicles 2-15 em ide lax. mostly open or narrow, со ovary pubescent ог glabrous:
culms glabrous below the inflorese ‘ence (Trisetum sect. Trisetum).

Ta. Lemmas (2.5-)2.74.3 mm long, smooth to slightly scabrous; apex of the lemma no ntate;
dorsal awn delicate, curve "s first glume 1.7-2.5 mm long; sec i glume 2.8-3. po n long:
lodicules truncate at the apex; endemic to Nuevo León, Mexic T curvisetum

Tb. Lemmas 4.3-6 mm long, strongly scabrous; apex of | в жене biaristulate; Eo awn not
delicate, geniculate: first slime 2.5-5 mm ones sec e glume 3.5—6.5 mm long: lodicules
lobulate at the apex: in. central Mexico to Pe . T. irazuense

Ob. Panicles 0.5—1.3(-2) em wide, spiciform or subspic iform; ovary glabrous; culms a ee nt below
the inflorescence.
За. Lemmas glabrous; glumes se die on the ke E not ciliate; awn slightly scabrous; paleas
gem on the kee ili (Trisetum sect. Trisetaera
Glumes shorter than the spike let, 1 05 de first l-nerved, the second 3-nerve ес. ligule

0.5-1 mm long; plant not rhizomatoi T. spicatum
9b. G lumes as long as the spi нет Mie ан (1)3-nerved, the second (3)5- -ne I ligule
—4 mm long: plants rhizomatot T. ligulatum
b. Lemmas ss scent; glumes se 1 or ciliate on the keel; awn sc 'abrous or lie: рага is
ш r ciliate on the keels.
10 Cs c E on the keel and slightly shorter to as long as or longer than the spikelet;
first glume 3.7-6 mm long, ovate-lanceolate; second кн 1.5—6.5 mm long. ovate-
lane со to ovate; le mma awns plumose; paleas ciliate on the keels 9. T. rosei

10b. Glumes somewhat scabrous on the keel and shorter than the spikelet (about 24 the
length): first glume 3-3.2 mm long, linear-lanceolate: second glume about 4 mm long,
line ur- абсеоіаќа to lanceolate; lemma awns not plumose, but ciliate near the base
paleas scabrous on the keels 6. T. 5
5b. Awn inserted on the lower third or near the middle of the lemma: glumes subequal, nearly as long as
1 ıe spikelet or longer; lemma with apical teeth without prolongation of the intermediate nerves or with
2 to | setae; lemma rounded in cross section; palea sometimes enclosed by the margins of the lemma,
not pias (Trisetum subg. Deschampsioidea ).
lla. Spikelets 2-flowere ы panicles narrow, subspiciform to spiciform, 0.6-2(4) em wide.

12a. Glumes equal in length and longer than the spikelet: spikelets 7.5-9 mm long: re mmas
bidentate at the apex; panicles 1.5-2(4) em wide, a with purple and gold; ovary with
trichomes at the apex 11. J. macibargensaleñas

12b. Glumes subequal, shorter than the spikelet; spikelets 6.5-7 mm long; lemmas with four

setae at the apex; panicles 0.6-1 em wide, green: ovary glabrous at the a pex
13. T. pinetorum
IBI ee 2- to 6-flowered; panicles open. lax, (1—)2—20 em wide.
За. Culms 150-300 em tall, bambusiform, 5-7(-10) mm diam. below: lemma apex 2- or 4-
— or -toothed, sometimes appearing almost entire, the lateral nerves do not contain

s (vascular tissue 17. T. virletii
13b. C m — 50 em tall, herbaceous, usu: Шу less than 4 mm diam. Бе low: lemma apex 2-
lobed, or 4-awned due to the projection of intermediate and marginal nerves (setae) beyond

the apex.

Ida. Lemmas dorsally hirsute below the awn insertion: ovary with trichomes at the apex

T. durangense

14b. Lemmas glabrous or dorsally scabrous: ovary glabrous, rare ‘ly pilose (see T. martha-
gonzaleziae).

лм,

Volume 91, Number 1
2004

Finot et al. 11
Trisetum, Peyritschia & Sphenopholis

15a. Lemma apex 2-lobed and 4-awned as teeth or setae
l6a. Lemmatal awns borne above the middle of ilie lemma.
Та. Lemma apex with four setae, the setae 0.6-1 mm 8 paleas slightly

shorter than the lemma;

callus trichomes 1.2-1.7 mm long

—

БЕРЕРИ 1 tonduzii

17b. Lemma apex sibus p setae; є baleen as long as or ni langer
than the lemma; callus trichomes 0.5-1 mm long or les

lob. nig awns borne near the aiddi or on lower М or 4 o
18 11

Ligules 3-6
lemma:
L

poar

18b.

tric ae 8 1.5-
15b. Lemma apex 2-lobed 1 any additional awns or setae.
19а. Spikelets (4)5- to 6-flowered __
I9b. Spikelets 2- or 3-flower
20a. Ligules 3-6 mm long: rachilla trichomes 0.5—1(-1.4) mm long
2

3) mm he ава shorter than the lemma: rachilla
16.

vd daban
X the lemma.
bre icu as long as or slightly longer than the

5 ; 2. T. palmeri

| long ꝛñ ñ— T. viride

14. T. spellenbergii

«d.

T. palmert

20b. L icula s 0.5-1(— 2)n mm » long rac hills trichomes 1.5-3 mm long.
21а

Glumes 7.5-9 m

cles 1.5—

21b.

iele 52-8 cm wide. open or somewhat mtract

1. Trisetum angustum Swallen, Phytologia 4(7):
423. 1953. TYPE: Marcos:

between San Sebastián and summit of Volcán

Guatemala. San
Tajumulco, on top of dry ridge in pine forest.
13 Feb. 1940, J. A. Steyermark 35525 (holo-
type, F-1040546!: US-2236479 frag-

ment & photo ex F!).

isotype,

Perennial; culms 12-24 cm tall, glabrous, dense-
ly caespitose. Leaf sheaths glabrous or pubescent
below; ligule 1.5-2.2 mm long: blades 3-8 em

| mm, flat. glabrous or sparsely pilose. Panicles
1-11 X 0.6-1 cm.
branches closely appressed. Spikelets 4.6-0 mm

narrow, densely flowered. the
long, 2-flowered; rachilla sparsely pubescent, the
trichomes about 0.6 mm long; glumes shorter than
first glume (2.7-)3—4 mm
long, l-nerved; the second glume 4—5.8 mm long,

the spikelet, unequal;

3-nerved: lemmas (lowest) 4-4.8 mm long, sca-
brous: apex irregularly toothed to 4-dentate, muti-
cous or with a short subapical mucro; the mucro up
to 0.5 mm long; callus obtuse, short pubescent, the
trichomes 0.2-0.6 mm long; anthers 0.8-0.9 mm
long. Caryopses ca. 2.1 mm long: endosperm solid,
hard.
Distribution. This species was described from
a Guatemalan specimen by Swallen (1953). A spec-
imen from Chiapas, Mexico (Matuda 2542a). was
cited in Pohl and Davidse (1994): however, we were
not able to study this. This species was not cited
for Mexico by Hernández-Torres and Koch (1988
but was included in Espejo-Serna et al. (2000).

—

Comments. The above description ts based on

G lumes 37 mm x long; 1 unequal, shorter than the и let:

n long. equal, longer than the spikelet: pani-
A) em wide, contracted, subspic iform: ovary pilose
ite: 11. T. martha- has aleziae

ee
16. T. viride

the study of type material and includes the descrip-
tion for Trisetum angustum given by Pohl and Da-
vidse (1994), who also studied the holotype. This
species appears closely related to T. pringlei. Pohl
and Davidse (1994) suggested that T angustum
might be better treated as a variety of J. pringlei
since these species are morphologically very simi-
lar. Both species have obtuse lemma apices and
lack well-developed awns. These characteristics do
not correspond well with the generic characteristics
of Trisetum. Therefore, we consider the systematic
position of these two species to be tentative or pro-
visional. We have placed T. angustum and T. prin-
glei in Trisetum subg. Trisetum but have not as-
signed them to a section (see Appendix 1).

2. Trisetum curvisetum Morden & Valdés-Rey-
na, Brittonia 35: 375. 1983. TYPE: Mexico.
Nuevo León: Zaragoza, Sierra Madre Oriental.
Ejido La Encantada, sitio La Tinaja, 1 km N
del aserradero, ca. 23°55'N, 99°45’ W, 2830 m.
25 July 1981, Valdés-Reyna & Capó VR-1419
(holotype, TAES not seen; isotypes, ANSM not

¿NC MEXU not seen, MO-

TEX not

XALU not

seen, ENCB not seen,
3102085 not seen,
US-2978399!.

NY not seen,
seen, UT not seen,

seen).

Perennial, with short rhizomes; culms 50-150
em tall, glabrous, weak: nodes 4, glabrous. dark.
Leaf sheaths shorter than the internodes, glabrous
to sparsely pubescent or only ciliate on the mar-

gins; ligule 1.1-2.5 mm long, membranous, oval.

Annals o
Missouri Botanical Garden

ciliate or denticulate; blades (5-)9-20 em X 1.5-
8.5 mm, flat, glabrous or sparsely pubescent on the
adaxial surface. Panicles 11—30(—36) х
ax, mostly open, pyramidal, paucispiculate, rachis

2-15 cm.

glabrous: pedicels 0.5—4.5 mm long, scabrous to-
ward the apex; the branches flexuous, in verticels
of five, ascending. widely spaced below becoming
crowded near the apex. Spikelets 3-5.2 mm long,
(1)2- or 3-flowered: rachilla 1-1.8 mm, glabrous to
scabrous, sometimes with a few trichomes at the
apex; glumes shorter than the spikelet, unequal,
margins hyaline, apex acute, scabrous on the keel:
first glume 1.7-2.5 mm long. linear-lanceolate, at-
tenuate, I-nerved; second glume 2.8-3.8 mm long,
lemmas (2.5—)2.7—4.3

mm long, lanceolate, laterally compressed, slightly

ovate-lanceolate, 3-nerved;
keeled, awned, 5-nerved, the nerves conspicuous,
glabrous to scabrous, slightly bidentate at the apex
or the apex entire, the margins and apex hyaline:
awn 3—5.5 mm long. borne on the upper М or Y.
less than 1 mm from the apex, flexuous, delicate,
curved, scabrous; callus obtuse, glabrous or sparse-
ly pubescent, the trichomes ca. 0.1 mm long: paleas
2-3.1 mm long, hyaline, shorter than the lemma.
2-nerved, the nerves scabrous, acute at the apex:
0.2-0.3 mm He an-

lodicules oblong truncate,

or 2 short,

thers 0.5-1 mm long; ovary with 1
curved and shining trichomes on the apex. Cary-

opses 1.7-2.2 X 0.4-0.6 mm; endosperm soft.

Chromosome number. 2n
res & Koch, 1988).

Anatomy and micromorpholog y.

— 28 (Hernández-Tor-

Ligule apices
composed of papillose cells: trichomes absent: lig-
ule epidermis more or less rectangular, short, with

straight walls; prickles and macrohairs absent. Leaf
sections flat; keeled and well Жан adaxial
ribs absent; bulliform cells in fan-shaped groups
between vascular bundles: eat epidermis com-
posed of fusiform long cells, with straight walls:
prickles present: short cells present both in costal
and intercostal zones; stomata present only in ab-
axial epidermis.

Distribution. Endemic Mexico, known only
from Nuevo León, 2100-2500 m.
Comments, Although the occurrence of oblong

truncate lodicules in Trisetum curvisetum is unusual
in the genus in comparison with the typical form
(lobulate to irregularly lobed or toothed) in the ge-
1983),

characters seem to pose questions as to the generic

nus (Morden & Valdés-Reyna, no other

position of this species. The presence of short,
curved, and shining trichomes on the apex of the
ovary and caryopsis confirms its generic. position.
The habit of the plant, the structure of the panicle,

the morphology of the spikelets, the presence of
trichomes on the ovary, and caryopsis shape all
suggest an affinity with 77 cernuum.

арР studied. MEXICO. Nuevo León: Zarago-
чта Madre Oriental, 7 7 km SE antes de La Encan-
Zaragoza-Ejido La Ene antada,
25 July 1981. J. Valdés-Reyna & M.
Сард VR- 1417 (US-297 a Paratype) ca. 15 mi. SW of
ramberri, 24702'32.2"N, ‚ 20 Sep. ~
se et al. 16719 (/ I i: DUC US): ca. 17 mi.
of des rri, 20 Sep. 2002, Peterson et al. 16723 ( peed
‘ONC, US): Sitio La Encantada- he Tinaja on road to La
1 1 23°53’ 14.4" N, 99°47'44.2"W, 21 Sep. 2002. Pe-
terson et al. 16764 (ANSM, CONC. US)

N
=
H

a

За. Trisetum filifolium Scribn. ex Beal var. fili-
2: 375. 1896.
TYPE: Mexico. Chihuahua: cool slopes of the
Sierra Madre. 9000 ft., 3 Oct. 1887. C. G.
Pringle 1431 (holotype, US -8177 3
CM not seen, US-825600!).

folium, Grasses N. Amer.

isotypes,

Perennial, caespitose, rhizomes absent; culms

30-60 em tall,
scaberulous, o

glabrous. Leaf sheaths oo

г pubescent: ligule (0.2—)1—3.5 mm
long. ШЕ idee a truncate, glabrous or with short
trichomes; blades 5-22 cm X 0.5-2 mm. involute.
filiform, curved and flexuous, glabrous or slightly
scabrous. Panicles 12-15 X 2—3 сш, lax. somewhat
open, narrow, exserted; the branches semiverticil-
late, the half-whorls with 3 to 7(8) branches. the
lower ones 4-6 cm long; rachis glabrous. Spikelets
3.5-6 mm long, (1)2- or 3-flowered: pedicels sca-
brous: rachilla 1—1.2 mm long, with trichomes са.
1.5 mm long. the trichomes longer at the apex:
glumes subequal, shorter, slightly longer, or about
as long as the spikelet: first glume 2.5-6 mm long,
1(3)-nerved, second glume 3-7 mm long. 3-nerved:
lower floret 3.5 mm long: lemmas 3.5—5 mm long,

obscurely 5-nerved, strongly scabrous, sometimes
scabrous-pubescent, terete, the margins involute
enclosing the palea: apex entire or shortly bilobed,
each lobe with two short teeth, muticous or with a
short subapical muero: mucro 0.2-0.5 mm long:
callus pubescent or subglabrous, obtuse, trichomes
са. 0.2 mm long: paleas 34.5 mm long. shorter
than the lemma, enclosed by the involute margins
of the lemma (not gaping), 2-keeled, the keels well
apart, ciliate or conspicuously scabrous: lodicules
with acute apex and a lateral lobe below the mid-
dle, 0.4—0.5 mm long: anthers 1-2 mm long: ovary
glabrous. Caryopses 1.5-2 mm long: endosperm
soli
Anatomy. Leaf blades in transverse section are
without a well-developed keel and with prominent
ribs; furrows more than one half of the leaf thick-

Volume 91, Number 1
2004

Finot et al. 13
Trisetum, Peyritschia & Sphenopholis

ness; sclerenchyma present as a continuous abaxial
band, adaxial girders T-shaped, marginal scleren-
chyma present; adaxial epidermis has trichomes
and inconspicuous bulliform cells: the abaxial epi-
dermis lacks trichomes or prickles.

Endemic to Chihuahua, Durango
2001). and Hidalgo.

Distribution.

errera- Arrieta, Mexico.
1600-3100 m.

Comments.
ical Trisetum species by having a terete lemma (vs.

Trisetum filifolium differs from typ-

lemma keeled), the lemma apex entire or bilobed
(vs. 2-aristulate to 2-dentate in Trisetum). the palea
enclosed by the lemma (free from the lemma in
Trisetum). and by having linear lodicules (vs. 2 or
3 lobate at the apex in Trisetum).

7 a studied. MEXICO. Chihuahua: Sanchez.
12 Oct. 1910, Hitchcock 7682 (US); 27.6 mi. NW of Ro-
che ү? Е оп road to Basigochi, 19 Sep. 1991, Peterson el
al. 97 (US). Hidalgo: Zacualtiplán. trailside, slopes
& ravines by Río P Е between Zacualtiplán & Olotla
on road to Metztitlán, 3 Jul y 1947, Moore 3250 (US).

KEY TO VARIETIES OF TRISETUM FILIFOLIUM
the mucro 0.2-5 mm long,
3a. Т. ‘Allin v var. filifolium
. Lemmas ташы. the awn 3—
late and twisted, borne on бе иррег third of the
lemma, i.e.. inserted е the apex
(—— T. filifolium var. aristatum

la. Lemmas mucronate,
inserted apically
1 long, genicu-

—

. Trisetum filifolium var. aristatum Scribn.
ex Beal. Grass. М. Amer. 2: 375. 1896. TYPE:
Mexico. Chihuahua: cool slopes of the Sierra
Madre. alt. 9000 ft.. 7 Oct. 1887, C. G. Pringle
1430 (holotype. US-868411!: isotypes, MO-
3727972 not seen, NY not seen).

دن
—
=

Distribution. Endemic to Mexico in the Sierra
Madre Occidental in Chihuahua and Durango and

Sierra Madre Oriental in Coahuila. México, and Hi-

dalgo (Hernández-Torres & Koch, 1988; Finot,
2003b).
Comments. ‘Though Beal (1896) suggested that

variety aristatum could be a different species, the
overall morphology of the plant and the structure
of the spikelets conform with the general descrip-
tion of Trisetum filifolium.

MEXICO. Durango: 3.2 n

Specimens sl udied. of
2003. Ped.
ea

La Pefia on road toward La Puerta, 15 Sep.
et al. 17785 (CHDIR. US).
Puerto Ing. н Diaz. km 230-235 on hwy. between
Zimapán & Jacala, 7 July 1948, Moore & Wood. Hs 3765
(US). México: 28. 3 mi. NE of Temascaltepec on Mex
towards Toluca, 7 Oct. 1991, Peterson & locals 11084
(US).

4. Trisetum irazuense (Kuntze) Hitche.. Proc.

Basionym: Ca-
PL

Biol. Soc. Wash. 40: 82. 1927.
* irazuensis Kuntze, Revis. Gen.
2: 763. 1891. TYPE: Costa Rica. Volcán lrazü,
3000 m. a 24 June 1874. C. E. О.
Kuntze 2334 (holotype, NY-346300 ех Herb.
Kuntze!).

Trisetum 5 Hitche., Contr. U.S. Natl. Herb. 24:
358. 1927. TYPE: Colombia. Cauca: collected below
Pitayó, Rio Palo Basin, Tierra Adentro, 2400 m. Feb.
1906. H. Pittier 1435 (holotype, US-53 1631).

Trisetum scabrivalve т Revista Colegio Nac. Vicente
а afuerte 11: 8 t, 88 (Reprint 32, 36), 1930. TYPE:

ador. Crece en los pajonales del Pichincha, Pa-
ai (Pifo), Chimborazo y El Altar (type not lo-

cate
Trisetum iE. Fourn., Mexic. Pl. 2: 108. 1886. hom.
non Trisetum gracile (Moris) Boiss. Trisetum
fournieranum Hitche., Contr. U.S. Natl. Herb. 17:
326. 1913. TYPE: “San Luis de Potosí,” M. Virlet
d'Aoust 1382 (lectotype. ا‎ here, P!; isotype.
US-72697 1b fragment ex P!).

illeg..

Perennial, culms 75-100 cm tall,

glabrous, up to 2 mm diam. on the lower inter-

caespitose;

nodes; nodes 3. glabrous. Leaf sheaths shorter or
slightly longer than the internodes, glabrous or pu-
bescent; basal sheaths pubescent; ligule 2—4 mm
long, membranous, pubescent to densely pubes-
cent, the apex truncate, dentate or ciliate: blades
20-30 ст X 2.5-6 mm, flat, glabrous or pube scent:
upper blades 5-10 cm long. Panicles (7—)13-25 X
(1-)2-5 em wide.

green and purple; rachis glabrous to sparsely pu-

lax, narrow, vellow-green to deep

bescent; the branches appressed and ascending.
Spikelets 4—7(-9) mm long. 2- or 3-flowered: ped-
icels 2-7 mm long. glabrous to sparsely pubescent,
sometimes scabrous; rachilla 1—1.7 mm long, cov-
ered with stiff trichomes, the trichomes 0.5-1 mm
long: glumes very unequal, shorter than the spike-
et; the keel scabrous on the upper half, the mar-
gins hyaline; lower glume 2.5—5 mm long, narrow,
linear, l-nerved, acute at the apex. half as long as
the spikelet; upper glume 3.5-6.5 mm long. lan-
ceolate to ovate-lanceolate, abruptly attenuate, 3-
nerved, % as long as the spikelet: lemmas 4.3—6
mm long, 5-nerved, the nerves inconspicuous to-
ward the base, strongly scabrous on the upper half,
green and purplish toward the apex, sometimes
with short trichomes toward the base: apex awned,
hyaline, biaristate or toothed, the apical awns ca.
0.5 mm long, conspicuous; awn (2.5-)5.5-8.5 mm
long. borne on the upper Y or 4, straight or twisted
and geniculate: callus obtuse, with short trichomes,
the trichomes ca. 0.2-0.3 mm long: paleas 3.2—1.6
mm long, slightly shorter than the lemma, hyaline.
2-keeled, the keels scabrous on the upper half, 2-
dentate to 2-awned at the apex: lodicules ca. 0.7

Annals of t
Missouri Botanical Garden

mm long, bilobed at the apex, the lobes acute; an-
thers (0.8—)1.2—1.8 mm long: ovary glabrous. Cary-
opses 2.2—3 mm long: endosperm soft.
Chromosome numbers. 2n
dez-Torres & Koch, 1988).

Anatomy. Leaf blades are flat in transverse sec-

28, 42 (Hernán-

tion, with rounded adaxial ribs: furrows less than
one half of the leaf thickness; first-order vascular
bundles with adaxial and abaxial girders; second-
third-
order vascular bundles with small sclerenchyma

order vascular bundles with adaxial girder:

strands; bulliform cells in fan-shaped groups at the
base of the furrows; abaxial epidermis with fusiform
intercostal long cells with straight side walls; sto-

mata not seen; prickles rare; trichomes present:
costal cork cells and silica bodies in pairs or short
rows.

Distribution. This species has been reported for

Mexico (Chiapas, Distrito Federal, Durango, Hi-
dalgo, México, Oaxaca. Puebla, San Luis Potosí.
and Veracruz), Costa Rica, Panama, Honduras, Co-
lombia, Venezuela, Ecuador, and Peru; 2700-3600
m (Pohl, 1980: Hernández-Torres & Koch. 1988:
Davidse et al., 1994; Finot, 2003b).
A lectotype (M. Virlet d'Aoust 1382)
P was here chosen to stabilize the name since
there was another syntype (Ё M. Liebmann 613)
cited in the original protologue by Fournier (1886).
A specimen of Liebmann 613 was not found at P.

Comments.

Specimens studied. COSTA RICA. San a eri e
upper slopes of volcán Irazú, 24 Fel 11 5
66035 (US); San José, S-SW of Cerro М Ыш 10 De
oes” Weston 3673 (CR). GUATE MAL ie ne
Типи ná, Sierra de los Cue ni imatanes, 6 July

48276 (US ae _MEXICO.

à 8. C. 26 971 ). Méx

g 1910. chek 1448 (P).

5974 (US):

895, no lh ctor

€ 5 Chiriquí ups ‘ano, 29 Sep.
(US), 29-30 Sep. 1911, Hitchcock Ey (S). PERU.

ra: 5 i1 E of 5 аА on road toward ' e

Mar. 2000, Peterson & Re "fulio- Rodriguez 15135 (US).

Feb. 55.

La

pen fir woods, Sierra
(P). PANAM
911. Hitchcock аг?!

as Cruces, 5 Oc

—

Piu-

3l

Trisetum pringlei (Scribn. ex Beal) Hitehe..
Proc. 82

Biol. Soc. Wash. 40: 1927. Ba-
roba diu pringlei ar

sionym: ex
Beal, Grasses N. 561. . TYPE:
Mexico. Oaxaca: summit of Sierra s San Fe-

lipe, 10.000 ft., 4 Aug. 1894, C. G. Pringle
4765 (holotype, US-822340!; isotypes, CM not
seen, ENCB not seen, MO not seen, Pl. US-
749287!, US-251958!).
Perennial, e 118 culms 2
brous; nodes (1)2 or 3

25-80 cm tall. gla-
. glabrous. Leaf sheaths gla-
brous or pubescent, sometimes only pubescent at

the apex, shorter or longer than the internodes,
sometimes one side extended above summit as a
sheath auricle: ligule 0.5-1.5 mm long, the apex
truncate to ovate, minutely denticulate and ciliate:
4-9(-12) cm X 2-5 mm. flat.

subinvolute, the lower blades glabrous or pubes-

blades sometimes
cent, ciliate on the margins, the upper blades gla-
Panicles 4—17 —12 cm, open, lax, usu-
ally purplish; branches up to 8 em long, verticillate,
capillary and flexuous: rachis glabrous to somewhat
scabrous. Spikelets 3.5-6.5 mm long, 1- or 2(3)-
flowered, pedicels up to 4 mm long,

brous.

capillary, g

a-
brous, purple: rachilla 1-1.5 mm long, with tri-
chomes 0.5-1 mm long. distributed toward the
apex: glumes unequal, shorter than the spikelet,
acute, the keel smooth or scabrous on the upper
half: first glume 1.4-2.6 mm long. linear-lanceo-
late, 1-
nerved; second glume 2-4.5 mm long. lanceolate,
3-nerved:

shorter and narrower than the second.

lemmas 2.6-4 mm long, strongly sca-
rous, sometimes covered by short trichomes, pur-
ple. terete, 5-nerved, the nerves conspicuous to-
ward the apex: margins hyaline; apex truncate,
entire or mucronate; subapical mucro when present
less than 1 mm long: paleas 2.2-2.9 mm long.
shorter than the lemma, hyaline, 2-nerved, some-
times purple-tinged, the keels scabrous to ciliate-
callus obtuse, with tri-
chomes 0.1-0.5 mm long: lodicules 0.4-0.7 mm
long. linear, not lobed, the apex obtuse, ciliate:
apex rounded or acute; anthers 0.6-1.2 mm long:
ovary glabrous. Caryopses I. EI.) mm long. ca. 0.4
mm wide: endosperm solid.

scabrous on the upper half;

Anatomy and micromorphology. Leaf ligule
apex has only papillate cells and the epidermis is
composed of more

~

г less rectangular long cells
with straight side walls; hooks and prickle hairs
present; stomata Leaf blades in
transverse section are without a keel and have well-
developed ribs: furrows more than one half of the

leaf thickness. bulliform cells inconspicuous; vas-

were not seen.

cular bundles with both adaxial and abaxial girders
alternate with free bundles without associated scle-
renchyma, adaxial girder T-shaped, abaxial girders
I-shaped,

marginal tri-

chomes on both adaxial and abaxial surfaces. sto-

sclerenchyma_ present:
mata present on the adaxial epidermis; abaxial epi-
dermis composed of long cells with undulate side
walls: costal cork cells-silica bodies present, tri-
chomes present, prickles not seen.

Distribution.
la), Guatemala, Costa Rica, and Panama:
3500 m (Hernández-Torres & Koch.
2003b).

Mexico (Chiapas, Oaxaca, Pueb-
1500—
1988; Finot,

Volume 91, Number 1
2004

Finot et al. 15
1 950 Peyritschia & Sphenopholis

Comments. The number of florets in Trisetum
pringlei varies from one to three per spikelet. One-
flowered spikelets are infrequent in Trisetum, and
are found in some individuals of T. filifolium, T.
pringlei, and in the South American 7 ambiguum
Rúgolo & Nicora (Rúgolo de Agrasar & Nicora.
1988).

On the basis of morphological, anatomical, and
embryological characteristics, Hernández-Torres
and Koch (1988) concluded that this species be-
longs in Trisetum, as was proposed by Hitchcock
(1927). Trisetum pringlei differs from typical spe-
cies of Trisetum by having lemma apices that are
entire and mucronate, and linear lodicules with en-
tire (not lobed) apices. Further studies are needed
to clarify the generic assignment of T. pringlei (see
Appendix 1).

COSTA RICA. Cartago: along the
Pan dip Iwy.. Cerro de la Muerte, 8 Aug. 1972,
Taylor 11750 (US): Crater volcán lrazü. a Oct.
Anderson 1339 (US-2042177): Cerro de la

Specimens studied.

American Hwy., 5 km above Mill: Isville, UM ra de Ta-
m nca, 22 July 1949, кезе des Iltis 483 (P). San José:
ordillera de Talamanca, o de La Muerte, Asunción

summit, 13 July 1968, d € "Davidse 10694 ( CR). GU. A-

TEMALA. Huehuetenango: b b Ў

bluff. summit of Sierra de los Cuchumatanes, 6 Aug.

1942, Steyermark 50224

Chiu Jolán, mounts above Totonk
19

(US). Totonicapán: region of
ps i ау to Des-
Standley ). PANAMA
C hiriquí: C ШТ Mg 'ano, 2t E т E р: is l. Hite ба

228 (US). eo Jaxaca: bois of Sierra de San
Felipe. 4 i 89: кл. E : vicinity of Cerro
San Felipa, vi sli 1108 (US

consuelo, 2: И.

6. Trisetum barbatipaleum (Hultén ех Veld-
kamp) Finot, Contr. U.S. Natl. Herb. 48: 661.
2003. Basionym: Trisetum spicatum var. bar-
batipaleum Hultén ex Veldkamp, Gard. Bull.
Singapore 30(1): 135. 1983. Trisetum spicatum
subsp. tolucense var. barbatipaleum Hultén.

Svensk Bot. Tidskr. 53: 223.

1959, nom. inval.

TYPE: Mexico. Hidalgo: Trinidad Iron Works,
1770 m, 21 Aug. 1905, C. G. Pringle 10052

(lectotype. designated by Veldkamp, in Veld-
kamp & Van der Have (1983: 135). S not seen;
isotypes, C not seen, L not seen, PL SE.

162083!).

Perennial, caespitose; culms ca. 40 em tall, pu-

bescent; nodes pubescent. Leaf sheaths shorter
than the internodes, pubescent; blades ca. 7 cm X
1-2 mm. flat, pubescent abaxially, glabrous ada-
xially. Panicles 8-10 X 0.5-1 em, spiciform, in-
terrupted; rachis pubescent: pedicels pubescent,
Spikelets 5-5.2 mm long, 2-flowered: rachilla ca. |
mm long. pilose; glumes unequal, shorter than the
scabrous on the keel: first

spikelet, somewhat

glume 3-3.2 mm long, shorter and narrower than
the second glume, linear-lanceolate to lanceolate,
slightly longer than half of the spikelet, I-nerved;
second glume ca. 4 mm long, ovate-lanceolate to
ovate, 25 as long as the spikelet, 3-nerved: lemmas
3.5-5 mm long, pubescent, 2-aristulate at the apex.
awned on the upper third; awn ca. 6 mm long.
curved, divaricate, not geniculate or twisted, ciliate
near the base and scabrous above: callus with short
trichomes, the trichomes ca. 2 mm long: paleas
shorter than the lemma, ciliate toward the apex.
Lodicules ca. 1 mm long, bilobed at the apex; ovary
glabrous. Caryopses not seen.

Distribution. Endemic to Mexico where the
species is known only from the type locality.

Comments. Trisetum barbatipaleum differs from
T. spicatum in having conspicuously pubescent
lemmas. It is closely related to 7: rosei and differs
from the latter by having a narrower panicle,
glumes that are shorter than the spikelets and sca-
brous along the keel, and a first glume that is nar-
row and linear-lanceolate. Trisetum rosei has ovate
glumes as long as the spikelet, a wider and more
densely flowered panicle, glumes that are conspic-
uously ciliate on the keel, and a lemma with a plu-
mose awn.

1. Trisetum ligulatum Finot & Zuloaga, sp. nov.
TYPE: Mexico. Veracruz: La Perla, N side of
Pico de Orizaba, above the Piedra Grande
mountaineering shelter, 19503“ N. 97716'W,
4200 m. 21 Sep. 1986, M. Nee 33192 (holo-
type. SI!; isotype, CONC!). Figure 1.

Planta rhizomatosa, 13-30 em alta; culmi erecti, pilosi
vaginae pilosae; ligula 3—4 mm longa, Malina, truncata,
dorso pilosa: laminae planae 5-20 ст X 1-2.5 mm), pi-

losae; panicula spiciformis; spicula pa 5 mm le 2-

2

3-flora; glumae subaequales. inferiores (1)3-nervatae, su-
nata scabra, 5-nervata, ad
e biaristato; arista 2-3.5
reve pilosus; palea paulo brevior quam

—

ian (3)5-nervatae; lemi

—
~
=

‹ 1 superiorem aristata, apice

mm быз. callus b

lemma: lodiculae ad apicem 3-lobatae; ovarium glabrum.
Perennial, with short rhizomes; culms 13-30 cm

tall, erect. pilose below the panicle, the trichomes

antrorse above then retrorse below: nodes 1 to 3.

—

glabrous. Leaf sheaths longer than the internodes,
pubescent; ligules 3-4 mm long. dorsally pilose,
truncate: blades 5-20 em X 1-2.5

duplicate, pubescent. Panicles 5-9 X 0.5-1.2 cm.

5 mm. flat or con-

spiciform, green or purple; rachis densely pubes-
cent; spikelets 5-6.5 mm long. 2- or 3-flowered:
rachilla ca. 1 mm long, sparsely pubescent, the tri-
chomes 0.5 mm long; glumes subequal, nearly as
long as the spikelet, acute, the keel scabrous on
the upper half, green or purple: first glume 3.8—6

16 Annals of the
Missouri Botanical Garden

Mas, EAN

SS
Dh

—

=

ee a

B
Е
3
N
o
A
gure en id و‎ (Nee 353192). —А. Habit. —B. Sheath, ligule, and portion of the blade. C. Spikelet.
. Floret. —F. Palea, dorsal view. —G. Palea. lodicules, and stamens, ventral view. m Pistil.

mm long, as long as or shorter than the first floret, nearly as long as its lemma, scabrous on the keels:
(1)3-nerved: second glume 4.5-6.5 mm long. (3)5- — lodicules 3-lobed at the apex: anthers ca. 1.5 mm;
nerved; lemmas 4.3-6.5 mm long. scabrous, 5- ovary glabrous. Caryopses not seen.

nerved, keeled, awned: margins hyaline toward the

apex: apex biaristate: awn inserted on the upper Anatomy. Leaf blades in transverse section are
third, 2-3.5 mm long. curved. scabrous: callus without a keel and have well-developed ribs with
short pilose, the trichomes 0.5 mm long: palea furrows more than half the leaf thickness: bulliform

Volume 91, Number 1
2004

Finot et al.
Trisetum, Peyritschia & Sphenopholis

cells are inconspicuous, trichomes present only in
the abaxial epidermis, continuous abaxial scleren-
chyma band absent, vascular bundles of first order
without girders, bearing small strands of both ad-
axial and abaxial sclerenchyma. marginal scleren-
chyma present: stomata present in both adaxial and
abaxial epidermes; abaxial epidermis with rectan-
gular to fusiform long intercostal cells, short costal
cells solitary or in cork cell-silica body pairs.
prickle hairs present.

Distribution. This new species is known only
from the higher diesen (3810—4200 m) of Jalis-
co and Veracruz, Mexico

Comments. Trisetum ligulatum resembles T.
spicatum in having spiciform panicles and culms
pilose below the inflorescence. It differs from 7.
spicatum in having short rhizomes (vs. none), dor-
sally pubescent ligules 3—4 mm long (vs. glabrous
ligules ca. 1 mm long). spikelets with the first
glume 3-nerved and the second glume 5-nerved (vs.
first glume I-nerved and second glume 3-nerved,
and with both glumes nearly as long as the spikelet
(vs. shorter than the spikelet)

MEXICO. Jalisco: Nevado de Colima, 2t
mi. SW of Ciudad Guzmán and 14 mi. SW of paved hwy

Paratype.

ур road toward the Nevado, 23 Nov. 1995, P. M. Peterson
R. Blackburn 13778 (US
8. Trisetum rosei Scribn. & Merr.. Contr. U.S.

Natl. Herb. 8(4): 289. 1905. Trisetum rosei var.
tenerum Scribn. & . Contr. U.S. Natl.
Herb. 8: 289. 1905. "gs rosei Scribn. &
Merr. fo. tenerum (Scribn. & Merr.) Louis-Ma-
rie. Rhodora 30: 239. 1929. TYPE: Mexico.
Vole: ‘ап Popoc ow 3600 m. 7-8 Aug. 1901,
J.

—

Rose & К. : 6016 (holotype, US-
3958131: isotypes. ENCB not seen, MEXU-
4703 not seen, NY-431715 not seen).

Perennial, caespitose: culms 25-50 cm tall.

densely pubescent, the trichomes antrorse above
then retrorse below: nodes 2. Leaf sheaths glabrous
or retrorsely tomentose. shorter than the internodes;
ligule 1-2.5 mm long, scabrous on the dorsal sur-
face, truncate, conspicuously ciliate; blades 6-15
cm X 2-4 mm. flat, glabrous to pubescent on both
sides, soft or stiff. conduplicate or the margins in-
volute, the uppermost leaf blade 3—6 cm long. Pan-
icles 3 * 1-1.5 cm, subspiciform, dense. +
linear, acute at the apex, sometimes interrupted;
rachis pubescent. Spikelets 5-7 mm long, 2(3)-
flowered: pedicels up to 3 mm long: rachilla ca. 1
mm long, pubescent, the trichomes stiff, са. 0.5 mm
long: glumes slightly shorter to as long as or longer
than the spikelet, ciliate on the keel, the margin

hyaline, the apex acute, faintly tinged with purple:
first glume 3.7—6 mm long, lanceolate to ovate-lan-
ceolate, usually 1- or 3-nerved; second glume 4.6—
6.5 mm long, ovate-lanceolate to ovate, 3-nerved:
lemmas 4.2—6.2 mm long, pubescent, awned: apex
bisetulate and hyaline, seta 0.3—0.7 mm long: awn
2.5-5 mm long, borne on the upper third. plumose.
curved, not twisted or bent; callus obtuse, with tri-
chomes 0.3—0.5 mm long; paleas 3—4.5 mm long.
glabrous to pubescent, shorter than the lemma, 2-
nerved, the keels ciliate: apex bidentate, hyaline:
lodicules 0.5-1 mm long, 2-lobed at the apex, the
lobes unequal, acute; anthers 1-1.5 mm long; ovary
glabrous. Caryopses 2.5-2.7 mm long. ca. 0.6 mm
wide; endosperm liquid or soft.
Anatomy and micromorphology. Ligule apices
have short stiff trichomes, and the epidermis is
composed of more or less rectangular long cells
with straight side walls, hooks very frequent: no
Leaf blades in
transverse section did not have a keel but had well-

trichomes or stomata were seen.
developed ribs with furrows more than one half the
leaf thickness; bulliform cells inconspicuous; tri-
chomes present in both adaxial and abaxial epi-
dermes with a continuous abaxial sclerenchymatic
band present; first- and second-order vascular bun-
dles with adaxial and abaxial girders; adaxial gird-
ers T- or anchor-shaped; marginal sclerenchyma
present; abaxial epidermis with long cells with un-
dulated side walls, intercostal hooks and stomata
present, cork cells and silica bodies present in cos-
tal zones; no trichomes were seen in the abaxial
epiderm

a
México, Puebla, and Veracruz), between 2500 and
4300 m (Espejo-Serna et al., 2000).

Comments.

Guatemala and Mexico (Hidalgo.

Trisetum rosei was considered a
synonym of T. spicatum by Hernández-Torres and
Koch (1988). Trisetum rosei can be easily recog-
nized by its pubescent lemmas, ciliate glumes, plu-
mose awned lemmas, paleas with ciliate keels (vs.
lemmas glabrous, glumes scabrous, lemma awns
not plumose, and scabrous palea keels in J. spi-
catum), and, in cross section, an abaxial band of
continuous sclerenchymatous tissue (absent in 7.
spicatum).

e studied. GUATEMALA. Huehuetenango:

s Chuchumatanes, 6 July 1942. Steyermark

m ME XICO. Hildalgo: Inter Pachuca et Min-

eral del Chico, 20 Dec. 1931, зан & Hultén 3 (5):

mtns. above Pachuca, 4 Aug. 1 ] J >

tween Pachuca & x del ^ n 19
Rose. Painter & J. S. Rose 8686 (US). México: V

Ixtaccihuatl, media falda 13 Sep. 1953. Matuda 29044

(US); 24.2 km E of Amecameca & 2.5 km '

S of Paso de

Annals of the
Missouri Botanical Garden

10 Oct. 1991,

e

Cortéz. Pe 7 & Annable 11103 (
1958, Beaman oe (U n
Popoc ate E 5-6 iub 1910. E 87 (US): don
| 9 km E of San 1 16 July
Puebla: № side of Popocate-
1729a (US); ca. 1 km Paso
e UR Mt. Orizaba.
US): Mpio. San Ni-
1, Vol ‘ап Ixtaccihuatl, 7 km
n E Amecameca, 2
pee Koch 7623 1 (US); Mpio. de Tochimilco, du Cor-
7. Tlamacos, 16 km ESE de Amec n a, 18 Oct. 1976,
pan 762056 (US). Veracruz: Mt. Orizaba, 15 1908.
Purpus 3018 (BAF); Pico de Orizaba, N of Cueva del
Muerto, 21 Sep. 1957, Beaman 1778a (US)

side of mt. ca.
1959, ‘ama 2853 (US).

petl, Sep.
de C 1 z, 21 July 1
1910,

„д
—
~

Jet.

9. Trisetum spicatum (L.) K. Richt., Pl. Eur. 1:

59. 1890. Basionym: Aira spicata L., Sp. Pl.
Aira subspicata L., Syst. Nat. ed.
10 2: 873.
roides Koeler, Descr.

159, nom. Шер. superfl. Avena ai-

Gram. 298, 1802, nom.
illeg. superfl. Trisetum subspicatum (IL) P.
Beauv., Ess. Agrost. 88, 1812, nom. illeg.

superfl. Trisetaria airoides (Koeler) Baumg.,

Enum. Transsilv.

Stirp. 3: 265. 1816, nom.
illeg. superfl. Trisetum airoides (Koeler) P.

Beauv. ex Roem. & Schult., Syst. Veg. 2: 666.
1817, nom. illeg. superfl. Koeleria subspicata
(L.) Rehb., Fl.
illeg. superfl. Koeleria spicata Rchb. ex Wi

& Lange. Prodr. Fl. Hispan. 1: 72. 1861, nom.
inval. Trisetaria spicata (L.) Paunero, Anales
adrid 9: 516. 1959. TYPE: Swe-
Lapland: 1732, Linnaeus s.n. (lectotype,

Germ. Excurs. 30, nom.

designated by Edgar € Connor, in Edgar

(1998: 556). LINN-85.7!; isotype, Sh).

Avena tolucensis Kunth, Nov. Gen. Sp. 1: 148. dH Tri-
setum tolucense (Kunth) Kunth, Havin: Gram. 1: 101
t. 60. 1829. Trisetum spicatum acu
(Kunth) Hultén, Sve ШЕ 1 Bot. Tidskr.
ы PE: Mexico: "crescit in apricis, op ee ur-
bem mexicanam Тос а, alt. 1380 he Нит-
ae & Bonpland s.n. (holotype, P!; 5 8 BAA-
9 fragment ex Kl. BAA-3420 fragment ex Р!).
S n nivosum E. dapi кт PI. 2: 107. 1886. Tri-
setum spicatum var. ni n (E. Fourn.) bs MO
) 1928 1 10201 TYPE: Mexico. Ne-
vado de Toluca, Sep. 1865, Hahn s.n. (lectotype.
designated by juan аш 688), Pl: isotype, US-
fragment ex Р-Еош

2 ense
. 1959

Perennial, caespitose; culms 9—50 cm tall, erect,
densely pubescent below the inflorescence, the tri-
chomes antrorse above, retrorse below: nodes 1 or
2. Leaf sheaths 1—3(—6) cm long, glabrous: ligule
0.5-1 mm long, minutely denticulate; blades 1—4
em X 121.5 mm, flat, conduplicate toward the
apex, glabrous to pubescent, sometimes scabrous or
ciliate on the margins, the upper blade 1—5 em
2.5-1(-10) х 0.5-1.3(-2) em, spi-

long. Panicles 2

spicatum var.

ciform, green to purple, shining, usually interrupted
on the lower portions; rachis pubescent. Spikelets
1.5-5.5 mm long. (1)2-flowered: pedicels pubes-

cent; rachilla ca. 1 mm long with trichomes 0.5-
mm long: glumes subequal, wide, shorter than the
spikelet, or the first glume somewhat shorter and
narrower than the second glume, scabrous or more
rarely ciliate on the keel; first glume 3.7—4.8 mm
long, lanceolate to ovate-lanceolate, l-nerved; sec-

-—

ond glume 4.5-5.5 mm long, ovate, 3-nerved; lem-
mas 3.8—5 mm long, glabrous, purplish toward the
base, awned; margins hyaline; apex 2-aristate; awn
3.5-5 mm long. borne on the upper third or upper
fourth, geniculate to curved, sometimes slightly
twisted, scabrous, purplish; callus obtuse with tri-
chomes 0.3 mm long: paleas 3—4 mm long, free
from the lemma, shorter to slightly longer than the
lemma, hyaline, 2-nerved, the keels scabrous; lod-
icules 0.6 mm long, hyaline, 2-lobed at the apex:
ovary glabrous. Caryopses 2-2.8 mm long, ca. 0.6
mm wide; endosperm liquid.

Anatomy and micromorphology. Ligule apices
have long cells and papillate cells with trichomes
absent; epidermis with rectangular long cells with
straight side walls, without trichomes, hooks, or sto-
mata. Leaf blades in transverse section have prom-
inent ribs with furrows deeper than one half the
leaf thickness: adaxial and abaxial girders present:
marginal sclerenchyma present; adaxial epidermis
with inconspicuous bulliform cells; abaxial epider-
mis without trichomes and only few prickles pre-
sent

Distribution. Cosmopolitan and widespread.
Hultén (1959) and Clebsch (1960) gave a detailed
account of the distribution of Trisetum spicatum. In
Mexico and Central America T. spicatum is usually
found between 1900 and 4500 m

Comments. Trisetum spicatum has been consid-
ered a complex, with many subspecies or varieties
(Louis-Marie, 1928—1929; Hultén, 1959). Louis-
Marie. recognized 14 varieties and Hultén (1959)
divided J. spicatum into 22 тере laxa, in-
cluding 14 subspecies and 8 varieties. In a phe-
netic study, Randall and Hilu (1986) concluded
that the morphological variation is extreme and

-
-=

does not support the recognition of infraspecific
taxa. In this treatment we interpret 7! spicatum in
a stricter sense, revalidating T. rosei and raising T.
barbatipaleum to specific status.
However, T. spicatum remains an extremely vari-
able taxon with a large number of synonyms. In this
revision we have included only those synonyms that
occur in the study area, in addition to the basionym
and its nomenclatural synonyms.

Volume 91, Number 1
2004

Finot et al. 19
Trisetum, Peyritschia & Sphenopholis

DOMINICAN REPUBLIC. Distri-
to Nacional: Santo Domingo, Tierra de Oco
Azua. San José de Ocoa. Cuchilla del Pino n
Mar. 1929, Ekman 11214 (S): Cordillera Central, Prov. i
a е Pico del Valle Nuevo, 15 Oct. 1929, Ekman
13759 (S). oie Cordillera de Baharuco, LM чта de
Los о 29 Е g. 1926, Ekman 6803 (S). MEXI-
CO. Durango: in montibus prope
aguae stagni seu кы Aug. 1857, 0 ا‎ 57 (Р).
dales o: Sierra de Pachuca, 21 July 1901, Pringle 9603
5 Sep. 1958, Hernández
25 Sep.

Specimens studied.
Prov. ii

Convalli ma ani

Us). ud ө: Nevado de Toluca, 5

X 1019

т Pringle 4303 (S, 5)
19(

: Nevado de Toluca, en el « 70 05
Nevado de Toluca. crater,
. Diguet s.n. Mt. Popoc ано Hitchcock
59% с, Valle de V o, falda de Ixtaccihuatl, | May
Matuda ыш (US); Nevado de Toluca. \
lb Balls WE 5 (US): Volcán Toluca, 9 Sep. 1893, Nel-
son 17 (US : Таас C ‘ihuatl, above timberline. Oct.
sco: Nevado de Colima. 26 Aug.
. Orizaba. between
cakes and snow line, Mucha 6258 (US 5): Mt.
alpine region, Nov. 1906, Rose 1270 (US).

A
N

хы
со
>
®
—
a
=
=
e 8
a
E
E
№
e
~
NX
c

Orizaba,

10. Trisetum durangense Finot & P. M. Peter-
TYPE: - Me хїсо.

Madre Occidental, ' of Durango on
Hwy. 40, 2400 m, 29 Sep. 1988, P. M. Peter-
son & C. R. Annable 6034 (holotype, US!). Fig-

ure :

son. sp. nov. ‚ Durango: Sierra

Hs Sigs pilosae, inte odia paulo breviores vel aequale

—

anta perennis: culmi glabri vel scabri sub casi

ligula 3-67) mn
Аарне alae, Ше, 15-50 cm X
supra scabrae vel эра rse рне paniculae 15 a
20 cm. laxae: rhachis scabra: spiculae 7-9 т
2(3)- bu ume bee "n quam мйне ча contigua
gluma

боз acuta, lacerata; laminae con-

n longae.

minore 5; superior brevior angustior-

aristulata: callus pilosus; rhachilla pilosa. 2 mm longa:
palea 5.8-7 mm longa: lodiculae 0.7—1.1 mm longae: sta
mina 3: ovarium ad apicem breve pilosum.
„Perennial, caespitose, short rhizomatous: culms
—110 cm tall.

ы the panicle: nodes 3. pubescent. Leaf sheaths

glabrous or retrorsely scabrous be-

11-23 cm long. pilose, as long as or shorter than
the internodes, with the membranous margin on one
side sometimes projecting upward as long as a
sheath-auricle: ligule 3—6(—7) mm long. acute, lac-
erated above: blades 15—50 em X 1—4 mm, narrow,
flat to conduplicate, rigid. strongly scabrous on the
abaxial surface. scabrous and sparsely pubescent
on the adaxial surface, ciliate on the margins. Pan-
icles 15-22 X 5-20 cm. lax, drooping, open, py-
ramidal: branches appressed or ascending to
spreading 0 to 75° from the culm axis, branches in
4 or 5 verticillate whorls per panicle, each whorl
composed by 4 to 6 branches, apical branches 3—
7 em long. the lower branches 8—14 cm long: ra-
chis. branches and pedicels strongly scabrous, cap-

illary, bearing spikelets on the distal ends.
Spikelets 7-9 mm long. 2(or 3)-flowered: glumes
equal to subequal, similar in shape, as long as the
spikelet or slightly shorter than the spikelet (first):
first glume 5-6 mm long, lanceolate, slightly short-
er and narrower than the second glume, 3-nerved.
scabrous on the keel, apex acute: second glume 6—
9 mm long. lanceolate, 3-nerved, apex acute: lem-
mas 7-8 mm long. awned near the middle. pilose
especially below the awn insertion, 5-nerved, the
nerves conspicuous toward the apex but vanishing
toward the base of the lemma: margins of the lem-
ma flat; apex 2-lobed, the lobes acute with the in-
termediate and marginal nerves prolonged into 4
short apical awns; awn 7—10 mm long. geniculate
and twisted, golden brown, exserted: callus pubes-
cent, the trichomes ca. 1 mm long; rachilla ca. 2
mm long, pubescent; paleas 5.8-7 mm long. hya-
line, 2-nerved, the nerves ciliate; lodicules 0.7-1.
mm long. ciliate at the apex; anthers 2-3 mm long.
curved trichomes; ovary ca. 1 mm long. covered
with short, curved and shining trichomes near the
apex. Caryopses 2-2.7 ca. 0.7 mm: endosperm
soft.

Anatomy and micromorphology. ligule apex
composed of trichomes and some papillose cells:
ligule epidermis composed of long cells with
straight walls; prickles absent on the dorsal surface.
only present at margins; macrohairs and stomata
absent. Transversal section of the leaf blade with
conspicuous adaxial ribs: vascular bundles with ad-
axial girders T-shaped; abaxial girders united form-
ing a continuous band of abaxial sclerenchyma; ab-
axial epidermis with macrohairs and abundant
prickles; epidermal long cells with undulate lateral
walls; short cells present in costal and intercostal
zones; stomata absent in abaxial epidermis.

Distribution. Known only from the state of Du-
rango, Trisetum durangense occurs in open pine for-
ests between 2400 and 2600 m.

Comments. Trisetum durangense is distin-
guished by its pilose sheaths; pubescent nodes:
strongly scabrous blades: panicle with rachis,
branches, and pedicels strongly scabrous: long, pi-
lose lemmas; and an ovary with short, curved, and
shining trichomes at the apex. The presence of
these apical trichomes on the ovary is found in sev-
eral taxa, including T. cernuum Trin. and J. canes-
cens Buckley from North America, and T. hirtiflo-
rum Hack., T. caudulatum Trin. var. correae Nicora,
and T. longiglume Hack. var. longiglume from
South America. Trisetum durangense is the only
species in subgenus Deschampsioidea with pubes-
cent lemmas and with an ovary with curved and

20 Annals of the
Missouri Botanical Garden

\ \ | Ji
NA ril
M UN 11,
M NN j
M | |
WN \' \ N
\ | |

| Y |

| |

—

SSS
==

—

Innable 6034). —A. Habit. —B. Inflorescence. —C. Sheath, ligule,
. First glume, dorsal view. —G. Second glume, dorsal view.
2). —L. Stamens (3). —

Figure 2. Trisetum durangense (Peterson & +
and portion of the blade. —D. Spikelet. —E. Floret. —F.
—H. Lemma, dorsal view. —I. Palea, dorsal view. —J. Palea, ventral view. К. Lodicules (

M. Pistil. —N. Caryopses (2).

Volume 91, Number 1
2004

Finot et al. 21
1 Peyritschia & Sphenopholis

shining trichomes near the apex. Trisetum duran-
gense appears closely related to T viride and can
be easily distinguished from the latter by possess-
ing pilose lemmas (glabrous in T. viride) and pu-
bescent ovaries (glabrous in T. viride).

Paratypes. MEXICO. ри Mpio. de Durango.

Parque El Tecuán, 58 km W of Durango, 20 Sep. 1984
F. Casillas, R. Flores & Е Ruiz 9 (CHDIR); 56 km W of
Mie on Hwy. 40 toward Mazatlán, 23%54'45.1
105501540. O W. 6 Oct. 2002, M. Peterson & L.

Brothers 16964 (CONC, US); ca. 28 mi. N of Unidos aoe
ceremos on road toward San Miguel de Cruce
24°17'49.8"N, 105?29'32.2"W, 7 Oct. 2002, P. M. Peter-
son & L. E. Brothers 16985 (CONC, US).

11. Trisetum martha-gonzaleziae P. M. Peter-

son & Finot, sp. nov. TYPE: Mexico. Durango:

El Mezquital, 25 km de Los Charcos por ca-

mino a La Guajolota, 2110 m, 14 Mar. 1985.

M. González-Elizondo et al. 1645 (holotype.

CHDIR). Figure 3.

Planta perennis: culmi glabri, striati, 3-nodi, 75—100

cm alti; vaginae glabrae, striatae, quam internodia brevio-

; ligula 0.5-1 mm, ovata: laminae planae vel 77

ae, ages cn panicula contracta, acuta, 10-20 X 1.5-2(—

4) em: spiculae biflorae (triflorae). 7.5-9 mm pen

glumae « mm; lemmata glabra ad
apicem bidentata: callus pilosus: ovarium pilosum.

quales, 7.5-9 X 0.8-1.1

Perennial: culms 75-100 cm tall, glabrous. stri-
ate, nodes 3. glabrous, dark. Leaf sheaths 3-10 cm
long, glabrous, striate, shorter than the internodes,
ciliate on the margins near the summit; ligule 0.5
ovate,

long, vegetative culms,

mm
slightly cleft at the apex, minutely denticulate-cil-

longer in

iate at the apex, glabrous on the dorsal surface:
blades 10-30 em X 2-3.5 mm,
stiff, scabrous on both sides.

1.5-2(-4)

tinged with gold and purple, the branches semi-

flat or convolute.
Panicles 10—20 X
em, contracted, subspiciform, acute,
verticillate, each whorl composed of 5 or 6 branch-
es, the lowest branch up to 5 cm long; rachis gla-
Spikelets 7.5-9 mm long. 2(3)-flowered:
pedicels glabrous; rachilla 1.4-1.5 mm long,
densely pubescent, the trichomes ca. 1.5 mm long:
glumes 7.5-9 mm long. 0.8-1.1 mm wide, equal,
longer than the spikelet, weakly purple at the base,
yellow at the apex, the keel slightly scabrous, the

brous.

=

apex acute; lemmas са. 5 mm long, glabrous, 5-

nerved, rounded in cross section, bidentate at the
apex. the intermediate nerves reaching the apex or
prolonged beyond the apex as very short hyaline
selae; awn ca. 5 mm long. inserted (1.5 mm from
the base) near the middle or lower third, strongly
twisted, geniculate, as long as the lemma; callus
obtuse, pilose, the trichomes 1-1.2 mm long: palea

ca. 5 mm long. about as long as or longer than the

lemma, 2-nerved, the nerves well apart, tinged with
purple and slightly scabrous: lodicules ca. 0.5 mm
long. bilobed at the apex: ovary pilose.

Distribution. Endemic to Mexico (Chihuahua
and Durango) between 2110 and 2450 m.

Parques. MEXICO. Chihuahua: 53 mi. W of Balle-
za and 5 . E of Guachochi, 19 Sep. 1991, Peterson et
al. 10784 (US). Durango: Mpio. El Mezquital. a 5 km
del a del camino de Charcos a El Mezquital, 19
Mar. ‚ O. García 82 (CHDIR); ге а ие
за терен, de Santa María Ocotän. Nov. . M. Gon
zález-Elizondo s.n. (CHDIR)

Etymology. This species honors the Mexican
botanist Martha González-Elizondo. collector of the

type specimen.

12. Trisetum palmeri Hitchc., Contr. U.S. Natl.
Herb. 17: 325. 1913. TYPE: Mexico. Durango:
Otinapa. 25 July-5 Aug. 1906, E. O. Palmer
342 (holotype, US-571365!; EHI.
MO-3056871!).

isotypes,

Perennial, culms 60-100 cm tall,
glabrous. Leaf sheaths glabrous or scabrous; ligule

caespitose;

3-6 mm long, truncate, dentate, conspicuously cil-
iate at the apex, glabrous on the dorsal surface: leaf
blades 10-20 ст X 1-3(25) mm,
stiff, scabrous, sometimes glaucous. Panicles 10—
20 X 2-6 cm, the
branches 4 to 6, verticillate, the branches in distant

involute or flat.

lax, open, somewhat narrow,
whorls: rachis and pedicels glabrous. Spikelets 5—
6.5 mm long, 2- or 3-flowered: rachilla ca. 2 mm
the trichomes 0.5-1(-1.4) mm
long: glumes subequal, both
glumes shorter than the spikelet, the margin hya-
line. the keel smooth or only slightly scabrous; apex
acute; 3.5-4.5 mm long,
slightly shorter and narrower than the second; sec-
ong, 3-nerved; lemmas 4—5.3

pubescent,

long,
linear-lanceolate.

first. glume | -nerved,
ond glume 4—:
mm long, somewhat fragile, translucent, terete, sca-
brous toward the apex, awned, the awn borne at the
middle or upper third, 5-nerved, the nerves con-
spicuous below and vanishing toward the apex, or
more rarely prolonged in 4 very short awns; apex
2-lobed, the lobes obtuse, sometimes erose; awn 5—
7 mm long, geniculate and twisted, exserted: callus
with trichomes, the trichomes 0.5-1
less; paleas 4—5.5 mm long, equal to slightly longer
than the lemma, free: anthers 2-2.5 mm long: ovary
glabrous. Caryopses not seen.

mm long or

Anatomy and micromorphology. ligule apices

have short stiff trichomes and some papillate cells.
epidermis with long cells rectangular to fusiform
walls, tri-

with straight side hooks present: no

22 Annals of the
Missouri Botanical Garden

if
°з D
A H »
re = E uini n gonzaleziae (Gonzalez “ а 1645). —A. Habit. —B. Sheath, Sio and portion of the
bla de. — C. Spikelet . Florets (2). —E. Floret. —F. Palea with rachilla, dorsal view. —G. Palea, lodicules, pistil,

and stamens, 1 view. ede Pistil.

Volume 91, Number 1
2004

Finot et al. 23
Trisetum, Peyritschia & Sphenopholis

chomes or stomata were observed. Leaf blades in
transverse section are without a well-developed
keel but have well-developed ribs: furrows more
than half the leaf thickness, bulliform cells in as-
semblages of 4 to 9 in fan-shaped groups at the
bottom of the furrows; trichomes present on the ad-
axial epidermis only: continuous abaxial scleren-
chyma band present; first- and second-order vas-
cular bundles with adaxial and abaxial girders, the
adaxial ones T-shaped, marginal bundles only with
adaxial girder; stomata present on adaxial epider-
mis only, marginal sclerenchyma present; epider-
mis showed costal/intercostal differentiation, hooks
both in costal and intercostal zones, cork cells and
silica bodies in pairs; no stomata or trichomes were

1.
Distribution. Endemic Mexico (Chihuahua,
Coahuila, Durango, Jalisco, Nuevo León, Sinaloa,

between 2700 and 3400 m (Espejo-
2000; Finot, 2003b).

Hitchcock (1913) pointed out that
Trisetum palmeri is closer to Deschampsia than to

—

and Sonora
Serna et al.,
Comments.

Trisetum; however, he described the species under
Trisetum on the basis of the glumes shorter than the

3

florets. Trisetum palmeri was synonymized with T.
viride by Hernández-Torres and Koch (1988), from
which it differs in having more rigid leaves and a
longer ligule (3-6 mm long). Trisetum viride has a
short ligule (0.5—1(—2) mm long).

MEXICO. Coahuila: 55.3 km SE

Specimens studied.

of Saltillo and 16.6 km SE of Jame on road to Sierra La
Viga. 26 Sep. 1990, Peterson et al. 10065 (US). Durango:

Sierra Madre poco 2 mi. N of Hwy.
| „ Peterson el al 13424 (U

СИН.

huana and 4.7 m. Mesa ы Clo ria, 11 Sep. 2003,

« E Sánchez-Alvarado 17743 (€ ae US).

uevo León: Sierra Madre Oriental, 11.4 mi. W of Die-

де; ‘ho de Marzo up road toward Cerro At 18 Oct.
5).

995. Peterson & Knowles 13.336

Peterson

13. Trisetum pacas Swallen, Phytologia
A(T): 424. TYPE: Guatemala. Quezal-
tenango: 9 Santo Tomas, 22 Jan. 1940, J.
A. Steyermark 34824 (holotype, F- 1048257 not
seen; isotype, US-2230478 ex Fh.

Perennial: culms 35-70 cm tall, glabrous. Leaf

sheaths glabrous. with the margin extended up as
a sheath-auricle 3 mm long. as long as or longer
than the ligule; ligule 2-3 mm long, hyaline, trun-
cate, the apex denticulate, glabrous on the dorsal
surface; blades 1-2 mm wide, flat, glabrous. Pani-
cles 8-15 X 0.6-1 em, spiciform, narrow, densely
flowered, interrupted, green; branches 1—3 cm long,
closely appressed and ascending: rachis glabrous

to slightly scabrous. Spikelets 6.5-7 mm long, 2-
flowered; glumes subequal, ovate-lanceolate, acute
at the apex, green, the margins hyaline, the keel
slightly scabrous, both glumes slightly shorter than
the spikelet; first glume 5-6 mm long, l- to 3-
nerved; second glume ca. 6 mm long, 3-nerved:
lemmas ca. 6 mm long, scabrous near the apex, 5-
nerved, awned from the middle or lower third, the
margins hyaline and involute below, the apex hy-
aline and deeply bidentate, with 4 hyaline setae
formed by the prolongation of the intermediate and
marginal nerves beyond the apex: awn 10—12 mm
long. geniculate and twisted; callus obtuse with tri-
chomes ca. 1 mm long; paleas 3—4 mm long, shorter
than the lemma and enclosed by the involute mar-
gins of the lemma; anthers ca. 1.5 mm long: ovary
glabrous. Caryopses not seen.

Distribution. Guatemala and Mexico. Espejo-
Serna et al. (2000) cited Trisetum pinetorum for
Chiapas, Mexico.

Comments. The above description is based only
on study of the type specimen at US and the orig-
inal description. However, the Latin paragraph of
the original description by Swallen (1953) men-
tioned 3-flowered spikelets, and the English para-
graph mentioned 2-flowered spikelets. Spikelets
with 3 florets were not found in the specimen ex-
amined. Though the subspiciform panicle of T. pi-
netorum resembles the species of Trisetum subg.
Trisetum sect. Trisetaera, this species has a lem-
matal apex with four setae, and the awn is borne
on the middle of the lemma.

14. Trisetum spellenbergii Soreng, Finot & P.
M. Peterson, sp. nov. TYPE: Mexico, Chihua-
hua: Mpio. Ocampo, Parque Nacional de Cas-
cada Basaseachic, 2100 m. on nearly barren

rock at overlook ca. 1 km S of Cascada, З Oct.
1986, R. W. Spellenberg, R. J. Soreng. R. Cor-
ral & T. Lebgue 8654 (holotype, US!: isotypes,
ESAHE!, ID!, К!, MEXU!, MO!, NMC!, RSA!,
SI!, TAES!). Figure 4.

Planta rhizomatosa; culmi 40—60 em alti, glabri; vagi-

nae барат puce ei ше E superio-

ae; laminae 20-30 ст X 2-3.5

Ф
YD

7-9 mm longae, 900 ee florae; glumae subaequales; gluma
inferior 5.5-6.5 X 0.3-0.5 mm, quam superior paulo bre-
vior, l-nervia; ann ma superior 05-7. 5 X 0.6-0.8 mm:
lemmata glabra, 5-nervia, apice Майпо; arista 8-12 mm
longa, ds medio inserta; callus pilosus: palea 3.5-5 mm
longa, quam lemma sua brevior; lodiculae ad apicem bi-

lobulatae, ciliatae; stamina 3; ovarium glabrum.

Perennial. with short rhizomes; culms 40-60 cm

24 Annals of the
Missouri Botanical Garden

IV Ñ ARTANGERIM 2004 lis E
f. \ \

Figure 4. Trisetum spellenbergii (Spellenberg. Soreng, Corral & Lebgue 8654). —A. Habit. —B. Inflorescence. —

C. Sheath, ligule, and portion of the blade. —D. Spikelet. —E. Floret. —F. First glume, dorsal view. —G. Second
gul | | g

glume, dorsal view. —H. Lemma, dorsal view. —I. Palea, ventral view. —J. Palea. dorsal view. К. Palea. lodicules.

and pistil. —L. Lodicules (2). —M. Stamen. —N. Pistil.

Volume 91, Number 1
2004

Finot et al. 25

8 Peyritschia & Sphenopholis

tall, geniculate at the base, glabrous; nodes 2 to 4,
glabrous. Leaf sheaths glabrous, longer than the in-
ternodes, the lower sheaths loose and pilose, the
upper ones open only at the apex; margins mem-
branous sometimes on one side projecting upward
as a sheath-auricle as long as the ligule: ligule 4.5—
6 mm long, scabrous on the dorsal surface: apex
deeply lacerate, without cilia: blades 20-30 cm х
2-3.5

scabrous above.

mm, flat, soft, glabrous on the lower surface,
with or without a few long tri-
chomes on the upper surface: uppermost culm leaf

blade 10—20 cm long. 2-0 cm.

lax. open, exserted; branches in 3 to 5 whorls of 2

"unicles 9-L

to 5 branches per node, each branch bearing spike-

lets to near the base; lower branches 3.5-5 cm

long. Spikelets 7-9 mm long, (4)5- or 6-flowered:
rachilla ca. 1.5 mm long, pubescent, the trichomes
1-1.5 mm long, the rachilla prolonged beyond the
uppermost floret bearing a reduced floret; glumes
5.5-7.5 mm long, shorter than the spikelet, green,
purple to the apex and margin; keel smooth or

slightly scabrous; first glume 5.5-6.5 mm long,

slightly shorter than the second,
glume 6.5-7.5 mm long; lemmas 4-6.5 mm long,

|-nerved; second

glabrous, conspicuously 5-nerved, awned; inter-
mediate nerves not extended as apical awns; mar-
ginal nerves vanish below the apex: apex bilobed,
the lobes each ca. 2 mm long; awn 8—12 mm long,
borne on the middle of the dorsal surface, twisted
at the base. geniculate, usually twice as long as the
mm

lemma: callus pubescent, the trichomes ca.
long: paleas 3.5-5 mm long. shorter than the lem-
ma. 2-nerved, the nerves scabro-ciliated; lodicules
1-1.5 mm long. the apex entire or with 2 short and
unequal lobes, ciliate: anthers 1.2-2.5 mm long:
ovary glabrous. Caryopses not seen.

Anatomy and micromorphology. Sheath ligule
apex is composed of long cells with a few very short
trichomes and the epidermis with prickles princi-
pally on the lower half and margins, no trichomes
or stomata seen. Leaf blades in transverse section
keeled. with prominent adaxial ribs, furrows be-
tween ribs more than one half the thickness: scle-
renchyma of first- and second-order vascular bun-
dles with adaxial and abaxial girders: adaxial
girders ‘T-shaped, abaxial girders [-shaped: margin-
al sclerenchyma present: epidermis with costal/in-
tercostal zones differentiated, the intercostal zone
only with long cells more or less rectangular with
straight side walls. and costal zone with cork cells
and silica bodies in short rows: adaxial epidermis
with short trichomes, bulliform cells inconspicuous:
abaxial epidermis with hooks, stomata present only

on the adaxial surface.

Distribution. Trisetum spellenbergii is endemic
to Chihuahua and Sonora, Mexico.

Comments. Trisetum spellenbergii is morpholog-
ically similar to T. viride but can be separated from
the latter species by the presence of rhizomes (vs.
absent in J. viride), its shorter stature (culms 40—
60 cm tall in 7: spellenbergii vs. culms 50—150 cm
tall). soft and glabrous blades (vs. stiff and glaucous
blades). spikelets with a greater number of florets
(4- to 6-flowered in T. spellenbergii vs. 2- or 3-flow-
ered), and lemmas with long bilobed apices (the
lobes ca. 2 mm long in T. spellenbergii vs. less than
0.5 mm long and bidentate).

Etymology. specific epithet honors Ri-
chard William Spellenberg (1940—) a Mexicophile
and plant systematist at New Mexico State Univer-
sity.

0. Sonora: Sierra т Occiden-
ward Yepachic,
1992, P. M.

Раво МЕХІС

tal, 9.6 mi. Е of Maycoba on Hwy. 16 t
To m, 28?26' 13"N, 108?33'05"W, 14 b
Peterson & C. R. Annable 12509 (US

15. Trisetum tonduzii Hitchc., N. Amer. Fl.
17(8): 558. 1939. TYPE: Costa Rica. Mount
Poás, 2460 m, Nov. 1896, A. Tonduz 10749
(holotype, US-358711!).

Perennial with rhizomes; culms 30-85 cm tall,
erect, glabrous. Leaf sheaths glabrous, usually with
trichomes at the apex, with one of the sides ex-
tended up as a sheath-auricle; ligule 1-3 mm long,
truncate, dentate, ciliate; blades 3-21 cm X 2-6
mm, flat or involute, stiff, glabrous, sae |
loosely pubescent above. Panicles : 2-10
cm, lax, open, ovoid-pyramidal, with E us gla-
brous branches, usually as long as wide, purple:
rachis glabrous; branches up to 8 cm long, densely
flowered above, verticillate, up to 7 per node.
Spikelets 4.5-6.5 mm long, 2-flowered: pedicels
elabrous, scabrous distally; rachilla 1-2 mm long.
pubescent, the trichomes 3 mm long: glumes 4-6.5
mm long, equal to subequal, nearly as long as the
spikelet. usually purple, acute or awn-tipped,
sometimes the first glume slightly shorter and nar-
rower than the second glume; first glume l- to 3-
nerved; second glume 3-nerved; lemmas 3.8-6 mm

anceolate, glabrous, awned, slightly scabrous,

long.
5-nerved, the nerves conspicuous toward the apex.
the intermediate and marginal nerves prolonged be-
yond the apex as 4 setae or teeth, the setae 0.6—1
mm long; awn 7—13 mm long, borne a little above
the middle, bent and twisted: callus pubescent. the
trichomes 1.2-1.7 mm long; paleas 2.8—5.7 mm
long. slightly shorter than the lemma, free from the
lemma: lodicules truncate at the apex: anthers 1—2

Annals of the
Missouri Botanical Garden

mm long, purple; ovary glabrous. Caryopsis 2 mm
long: endosperm soft.

Chromosome number. п = 14 (Pohl. 1980).
Anatomy. Leaf blades in transverse section are
without well-developed keels or well-developed
ribs, furrows more than one half the leaf thickness,
bulliform cells in groups of 4 or 5 arranged in fan-
shaped groups; trichomes absent in both epider-
mes; vascular bundles with adaxial and abaxial
girders, except the marginal bundles; marginal
sclerenchyma present: stomata present on the ad-
axial epidermis only; abaxial epidermis with inter-
costal rectangular long cells, costal short cells sol-
cork

present intercostally.

itary or cell-silica body pairs, prickles

Distribution. Costa Rica and Panama, 1500—
3500 m
Specimens studied. COSTA RICA. Cartago: 7 Aug.

1966, Dat iil & Pohl 842 (MO); Cantón = Orea 'amuno,
P. Cordillera Central, °58'49"N,
1995, Morales & wd hin 4801
CR): Crater of Vole ‘an Irazú, 7 Aug. 1966 Pohl & Cal-

), Pittier 13082 (US); Sommet du Poas.
E 841 (US): Potrero ie l alto, Volcán Poas, Nov. 1896,
eie 214 (US); Sommet du Poas,

1 (P). San José: Las Nubes, 20-22 Mar
le "38398 (US). PANAMA. Chiriquí: Chiriquí. 18 Mar.
1938, White 54 (MO)

16. Trisetum viride (Kunth) Kunth, Revis. Gra-

min. 1: 101. 1829. Basionym: Avena viridis
Kunth, Nov. Gen. Sp. 1: 147. 1816. Triseta-
rium viride (Kunth) Poir, Encycl. 5: 366.

1817. Deyeuxta viridis (Kunth) E. Fourn., Bull.
Soc. Bot. France 24: 181. 1877. TYPE: Mex-
ico. "Crescit in alta planitie Mexicana inter
Salamanca et Queretaro, 900 hexap.. Hum-
boldt & Bonpland s.n. (holotype, Pl: isotype,
US-865584 fragment ex P!).

Trisetum bosse Swallen, BD de 4: 423. 1953. TYPE:

Guatemala. Sierra de las as, E of Fine а Piamon-

E P rogreso, 11 Feb. 1952. J. A. Steyerr mark
US-1935005! кА US

13836 (holotype,
2208€ 306! ).
Desc joue mexicana Swallen, Bol. Soc. Bot.
. 1958. Trisetum mexicanum (Swallen) 5
m. 28: 233. 1979. TYPE
de Bravo, 1800 m. 21 Nov
(holotype, US-2119860!; iiie. MEXU not seen).

Me xico 23:

Perennial, caespitose: culms 50-150 em tall:

nodes 4, glabrous. Leaf sheaths shorter than the

internodes, glabrous or pubescent, ciliate at the
apex; ligule 0.5-1(-2) mm long, membranous; apex

1 X 2-6(-

usually flat, somewhat stiff, sometimes con-

obtuse, minutely ciliate; blades 14—35 «
9) mm,

volute, glabrous with the adaxial face glaucous, the
abaxial green. Panicles 12—30(—37) X 2-8 em, lax,
open or somewhat contracted, greenish to yellow-
ish; lower branches 5-16 cm long, ascending, ver-
ticillate; rachis glabrous. Spikelets 5-8 mm long,

N

- or 3-flowered; pedicels 1-3 mm long, glabrous;
rachilla 1.5 mm long, pubescent, the trichomes
1.5-3 mm long especially near the apex, the lower
portion subglabrous or pilose; glumes 3-7 mm long,
subequal, somewhat translucent; first glume 3-6
mm long, l-nerved, slightly shorter than the spike-
let; second glume 4—7 mm long, 3-nerved, equaling
or slightly longer than the spikelet; lemmas 4—7
long, glabrous, awned: bidentate, 5-

mm apex

nerved, the intermediate and marginal nerves
sometimes prolonged as 2 or 4 hyaline setae ca. 0.2
mm long; awn 5—10 mm long, borne from the mid-

dle

twisted:

to the lower third fourth, geniculate and
callus obtuse, pubescent, the trichomes
0.5-1 mm long: paleas 3-6 mm long, shorter than
the lemma, hyaline, 2-nerved, the keels scabrous:
anthers 1—3.3 mm long; ovary glabrous. Caryopses
2-2.5 mm long; endosperm liquid.

Chromosome number. 2n = 28 (Herrera-Arrie-
ta, 200

Anatomy and micromorphology. ligule apices
have papillate cells and short trichomes; epidermal
long cells elongated perpendicular to the vertical
axis of the ligule, rectangular, with undulate side
walls; no trichomes, prickles, or stomata were seen
in the epidermis. Leaf blades in transverse section
are without a well-developed keel but have well-
developed ribs, furrows more than one half the leaf
thickness, trichomes present only in the adaxial
epidermis; first- and second-order vascular bundles
with both adaxial and abaxial girders, the marginal
bundles with sclerenchyma in small abaxial
strands; abaxial epidermis with intercostal rectan-
gular long cells with undulate side walls, costal
short cells present as cork cell-silica body pairs,
sometimes solitary; stomata and trichomes not seen,
prickles present.

Distribution. Trisetum viride grows in Mexico
and Guatemala between 1500 and 3100 m. In Mex-
ico it occurs in the following states: Chihuahua,
Chiapas, Durango, Guerrero, Guanajuato, Jalisco,
México, Michoacán, Oaxaca, and Querétaro (Her-
nández-Torres & Koch, 1988; Espejo-Serna et al.,
2000; Herrera-Arrieta, 2001)

Comments. | Hernández-Torres and Engleman
(1995) more recently performed an anatomical sur-
vey of Trisetum in Mexico and they considered T
mexicanum a distinct species. They noted that T.
mexicanum could be distinguished by the size of

Volume 91, Number 1
2004

Finot et al. 27
Trisetum, Peyritschia & Sphenopholis

the bulliform cells, but no further morphological
characteristics were discussed. We choose to place
T. mexicanum as a synonym of T. viride.

Specimens studied. MEXICO. Coahuila: Sierra Madre
Oriental, ca. 5 km E of Saltillo (Las Palapas) up camino
de Quatro, 20 Sep. 2003, Peterson et al. 17863 ( ИН.
US). Durango: along Mazatlán-Durango hwy.. 3-15 kn
toward El Salto from the Sinaloa iex at E | Palmito,

3 Apr. 1965, Mc p е km № carretera
Durango-Mazatlán, 6 € 1978. Ed & Sánchez 78155
(US): San Ramón, 21 pend FE 1906. Palmer 128
(US): Sierra pe Occidental, 2.4 mi. N of о
N of hwy. 40, 25 Oct. 1995, Pot "lerson et E 13.

2 mi. N of Tepehuana on road toward Mezquit on

2003. Peterson & E Sánchez-Alvarado 17739 * m

US) Guerrero: entre Avusinapa y Petatlán,

1894, Nelson 2123 (US); Teotepec, 11 May 1939, BÉ
et al. 14795 (US). Oaxaca: Sierra de San Felipe. 18 Sey
1894. Pringle 4919 (P. US).

17. Trisetum virletii E. Fourn.. Mexic. Pl. 2
108. 1886. TYPE: Mexico. San Luis Potosí:
1851. Virlet 1304 (lectotype, designated by Fi-
not (2003b: 675). Р!: isotype, US-91219 frag-
ment ex P-Fourn. 247!).

ae PI. 2: 108. 1886.
lexico. In sylva de la desierta Vieja vallis
1865. E. Bourgeau 1304 (holo-
type, Ply 1 7H not seen, US-fragment ex P-

Fourn-248!; US- еш nt ex MPU-Fourn-248!).

Trisetum bambusiforme E. Fourn..
TYPE

Perennial with rhizomes: culms 1.5-3 m tall, 5—
1(-10) mm diam. below with extravaginal branches
on the upper nodes, glabrous, bambusiform. Leaf
sheaths minutely scabrous, longer than the inter-
nodes; ligule (2—)5—10 mm long, membranous, apex
obtuse to truncate the cilia

. laciniate. and ciliate,

up to 2 mm long; blades 30-45 cm X 5-13 mm,
flat. minutely scabrous. Panicles 20-45 х 5-12(-
20) em. lax, +

yellow-green; branches usually 10-15 em а long, ver-

open, pyramidal, dense, green or

ticillate: rachis glabrous. Spikelets 5-7.5 mm long.
(3)4- or 5-flowered: pedicels 1—4 mm d sca-
brous; rachilla 0.5-0.7 mm long. densely pubes-
cent, the trichomes 2—3.3 mm long, more numerous
at the

awned, the first slightly shorter and narrower than

apex; glumes unequal, acute to shortly
the second, both glumes shorter than the spikelet,
scabrous along the nerves; first glume (3—)4—5.1(—
6) mm long, linear-lanceolate to lanceolate, 1-
4—6(—8) mm long, lanceolate
3-nerved; lemmas 4—6 mm
long. scabrous, 5-nerved, awned, the nerves not

nerved; second glume
to. ovate-lanceolate,

conspicuous near the apex, somewhat rounded in
cross section, the margins hyaline toward the apex:
apex 2- or 4-dentate (sometimes appearing almost
entire), the teeth short not prolonged as setae or
awns; callus obtuse with a few short trichomes, the

trichomes 0.5-1 mm long: aun 1.5—4(—4.5) mm
long. borne on the upper third, geniculate, slightly
twisted: paleas 3.5—5 mm long, shorter than the
lemma, 2-nerved, the nerves scabrous; anthers 1.8—
2.5(-3) mm long. Caryopses 1.5-2.5 mm long: en-
dosperm liquid.

Chromosome number. 2n = 28 (Tateoka, 1962).
Anatomy and micromorphology. ligule apex
has long cilia and short hair: epidermis composed
of long cells with undulate side walls, with abun-
dant prickles; no trichomes or stomata were seen.
af blades in transverse section are without a well-
developed keel or ribs, furrows less than one half
the leaf thickness with trichomes present on the
adaxial epidermis only; vascular bundles with ad-
axial and abaxial girders; marginal sclerenchyma
as a small rounded strand, stomata present in the
adaxial epidermis only; bulliform epidermis pre-
sent; adaxial epidermis with rectangular long cells
with straight side walls, short costal cells present,
stomata absent, prickles present.

Distribution. Endemic to Mexico (Chiapas, Dis-
trito Federal, Durango, Guanajuato, Jalisco, Méxi-
co, Michoacán, Morelos, Puebla, Querétaro, San
Luis Potosí, and Veracruz (Espejo-Serna et al..
2000; Herrera-Arrieta, 2001; Finot, 2003b). Trise-
tum virletii grows in moist woods between 2000 and

3500 m.

У аце: Э See d. MEXICO. Distrito Fede ral: C er-
ro Gordo, Cerro Cautillo Grande,
Station, бит N and W of old hwy. 95, \
Iltis, Koeppen & F. Iltis 152 (US). Hidalgo: along Hwy.
105 between Pachuca and Tampico, Же inity of
del Monte, 20°08'N, 98°3'W, 27 Feb. 987,
non 65794 (Sl ex MO). Jalisco:
Volcán Colima, 19*38'N, 103%35'W, 31 Dec.
Guzmán & Nee 1065 (US); SE NS of Nevado de Coli-
ma, 2 Apr. 1951, McVaugh 11721 (US): N slopes of Ne-
vado de Colima, 2 Apr. 1949, m a 10161 (US). Méx-
ico: Mpio. Amecameca, cañada del cerro Venacho, 12 km
al E de Amecameca, 23 Dec. 1976, Koch 76337 (US);
vicinity of La Cima railroad opine on top of the Serjana
e Ajusco, 19°07'N, 99*12'W, 2 1963, Iltis Я Iltis
1671-a (US); Valle de Mexico, С. Tb ps 7 Jan.
1 20892 (US); pm Cerro Venacho, $ Feb.
953, Matuda et al. 28076 (US); Sierra de Las Cruces,
Я Арг. 1898, 3 zh (US); Ixtaccihuatl, p 1906,
Purpus 1612 (US); Temascaltepec, Mesón Viejo, 12 Jan.
1932, Hinton 2745 (US); "ин ca. Cerro Texaltepec, 3
km SSE de San Pablo Ixayoc y 13 km SE Texcoco, 9 Nov.
1975, Koch 75706 (US). Michoacán: vicinity of Morelia,
9 Feb. 1911, Arséne 5410 (US); cool slopes of mountains
near Patzcuaro, 21 Dec. 1891, Pringle 3970 (US); Coal-
comán, Barroloso, 3 Mar. 1941, Hinton 15747 (US): Mt
s itaro, 22 July 1941, Leavenworth & Leavenworth 1122
dedere e Tres Marías, 16 Dec. 1907, Pringle 15002
1995 5 mi. S of Morelos-Federal District border, 14 Mar.
1961, pee 4155 (US)

Mineral

С roat & Han-

Annals of the
Missouri Botanical Garden

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Volume 91, Number 1
2004

Finot et al. 29
Trisetum, Peyritschia & Sphenopholis

fication, and Information Retrieval. Version: 14th De-

cember 2000. анге ойнен eee
APPENDIX I. Subgeneric treatment of Trisetum in
Mexico and Central Americ

Trisetum

Species, incertae sedis: J. angustum, T. filifolium, T.

pringlei

Trisetum subg. Trisetum

Panicles spiciform or more rarely contracted to open.
Spikelets usually 2- or 3-flowered: glumes lanceolate, un-
equal 1 ia or E iib
: first glur

. shorter or longer than the
e 1(3)-nerved, usually shorter and nar-
rower e the. sec uen second glume 3(5)-nerved; lemmas
laterally

lanceolate, 1 or pilose, slightly keeled,

=
5
=
=
Y
Y
E
e
л
a

, the nerves к б beyond the
awned from the upper
third: awn оа a Даш or merely divaricate. some-
glabrous or with short and aes
trichomes at the apex.
brous or with short trichomes at the apex: endosperm La.
uid or more rarely solid.

2-dentate apex as 2 ог.

Caryopses compressed, soft, gla-

Trisetum subg. Trisetum sect. oe

Species: T. curvisetum, T. irazuen
Trisetum subg. Trisetum sect. сен taera Asch. &
Graebn.. Syn. Mitteleur. Fl. 2: 270. 1895. TYPE
Trisetum spicatum (L.) К. 9 Pl. Eur. 1: 59.
1890.
Panic spiciform, narrow, densely flowered: rachis
densely

pilose to pubescent below the inflorescence
Spikelets 2- to (2)-flow E
glumes unequal, ads shorter than the us let, some-

owered, rarely l- or
limes ogee
Species barbatipaleum, T. ligulatum, T. rosei, T. spi-

catum

Trisetum subg. Deschampsioidea RP phe Finot,
0

stat. nov. Basionym: Trisetum subs d
sioidea Louis-Marie, Rhodora 30(5 o 928.
ТҮРЕ: Trisetum palmeri Hitchc., b кз» i

ed here.

Panicles lax, open, rarely spiciform. Spikelets 2- to 6-
flowered; glumes 2, + equal, lanceolate. keeled, muticous,
glabrous, pre shorter than or equaling the spikelet:
first glume 1-nerved; second glume 3-nerved: lemmas lan-
ceolate, membranous, with the apex and margins hyaline,
glabrous or rarely hirsute, slightly rounded in cross sec-
tion, 5-nerved, the nervy pearing toward the apex
or rarely н ae the 2-dentate apex in (2) or 4
setae, usually aw from the middle: awn geniculate;
ovary usually оо or rarely with short trichomes at
the apex soft, usually glabrous,
rarely with short and shining trichomes at the apex.

Species: T. di
meri. 1. pinetorum.
T. virletii

Comments. & lectotype was chosen because Louis-
Marie (1928) cited two species without designating a type.

тез disap}

Caryo ses compre ssed,

irangense, T. martha-gonzaleziae, T. pal-
spellenbergii, T. tonduzii, T. viri

а

&

APPENDIX 2. Li:
names are eoa ad in bold and synonyms are
italicized.

st of names and synonyms. Accepted

sión Besser ex Schult. & Schult. f. = Trisetum

Agrostis obtusata (Michx.) Steud. = S. obtusata

Aira koelerioides de = P. тае
Aira mexicana Trin.
Aira obtusata Mic hx.

tusata

; uxioi
Avena == Kunth = S. interrupta а inter-
ta
е ll Kunth = T. mm
Arena у J. Pres] = P. deyeuxioides
Avena viridis = T. vir =
Calamagrostis irazuensis Kur

= Ts i iraz
po Buckley —

. s. inte NUM

subsp. interrup
Desc Dn Loslerioidts (Pevr.) Benth. = P. koelerioi-
des

Deschampsia mexicana Swallen — T. es
ое my у d = P. pri

olut mn P. 8
1 grac ilis Г B ра = Р, humilis
Deyeuxia triflora Nees = eyeuxioides
veuxia viridis (Kunth) E. Fourr A de
Eatonia annua Suksd. = S.
Eatonia densiflora E. Sn = S. obtusata
Eatonia obtusata (Michx.) A S. obtusata

Eatonia obtusata var. purpurascens Vasey ex Rydb. &
Shear = S. ob

usa
Eatonia кила уаг. к ИЯ Vasey ех L. Н. Dewey = S.
bt

obtusa
“e ola var. robusta Vasey ex Rydb. = S. ob-
Eatonia 5 Scribn. & Merr. = S. obtusata

atonia p (Vasey ex L. H. Dewey) Rydb. = S. ob-
do ben 8 E. Fourn. = P. koelerioides
glei Scribn. ex Beal = T. pringlei
ob ae a Trin. ex = = S. obtusata
Koeleria paniculat a Nutt. = S. obtusata
Koeleria spicata Rehb. ex a & Lange = T. spicatum
Koeleria subspicata (L.) Rchb. = T. spicatum
coeleria truncata (Muhl.) Torr. = S. ob
Peyrits oe К. Fourn.
Peyritschia deyeuxioides (Kunth) Finot
a FT humilis (Lou ي‎ not
Peyritschia koelerioides (Peyr.) E.
Peyritschia pringlei (Se 'ribn. i S. D. Koch
Poa obtusata (Michx.) Link — S. obtusata
Rebentischia Opiz — 7 set
Reboulea gracilis Kunth — S. obtusata
Reboulea obtusata (Michx.) A. Gray = S. obtusata
ша obtusata var. pubescens (Scribn. & Merr.)
obtusata
Fe strina qoe = um
мк pubescens рак = Т. spicatum
olis Scrib

Farw.

n dou 155 annua (Suksd.) A. Heller = S. obtusata
. ени » ibn.) Scribn. = S. interrupta

rup
Sphenopholis i interrupta (Buckley) Seribn
Sphenopholis interrupta (Buckley) Saiba subsp. in-
Sphenopholis interrupta subsp. californica (Vasey)
Scribn.
Sphenopholis obtusata (Michx.) Scribn.

30

Annals of the
Missouri Botanical Garden

Sphenopholis bead pp lo. purpurascens (Vasey ex Rydb. &
Shear) Waterf. = S. obtusata

Sphenopholis ома a lobata (Trin.) Scribn. = S

Sphe nopholis visa кше, pubescens (Scribn. & Merr.)
cribn. = Mus
Sphe порой dian var. qu (Trin.) Seribn. ex B.
tob. = S. obtusata
enl obtusata var. pom (Scribn. & Merr.)
cribn. ex B. L. Rob. = obtusata
Re uem dba 8 Merr.) A. Heller = S.
obtusata
Sphenopholis robusta (Vasey ex L. H. Dewey) A. Heller =
S. obtusata
Trisetaria airoides (Koeler) Baumg.
Trisetaria deyeuxioides (Kunth) Poir. = P. deyeuxioides
Trisetaria spicata (L.) Paunero = T. spicatum
Trisetarium Poir. = Trisetum
Trisetarium disi (Kunth) Poir. =

= Т. spicatum

S. interrupta
subsp. in

Жш bw (Kunth) Poir. = T. viride

Trisetum Pers

Trisetum ай. Deschampsioidea (Louis-Marie) Finot

Trisetum sect. Trisetaera Asch. & Graebn

risetum sect possa
Trisetum subg. Trisetum
Trisetum subsect. Desc hampsioidea Louis-Marie = Tri-
setum subg. ha idea

Desc pr

Trisetum airoides (Koeler) * Beauv. ex Roem. & Schult.
_ e»

аша ери (Е, Fourn.) Scribn. = P. koelerioides

Trisetum altum Swallen — T. viri

Trisetum angustum Swallen
Trisetum bambusiforme E. Fourn. — T. virletii
Trisetum barbatipaleum (Hulten ex Ve rem Finot
Trisetum فو بت‎ Vasey = S. interrupta subsp. ca
lifornica

risetum curvisetum Morden & Valdés-Reyn:
Trisetum deyeuxioides (Kunth) Kunth = P. d iode
Trisetum deyeuxioides var. pubescens Scribn. ex Beal = P.

deyeuxioides
Trisetum durangense Finot & P. M. Peterso
Trisetum elongatum (Kunth) Kunth = S. interrupta
subsp. pta
Triseti tum dum (E. Fourn.) Hitche. = P. deyeuxioides

Trisetum filifolium Scribn. ex Be:
Trisetum filifolium Seribn. ex Beal var. filifolium

Trenit filifolium var. aristatum Seribn. ex Beal
= T. ir

—
>=
A.
z
&
~
=
=
i
=
~
8
>
=
pa
=
=
=.
D
=
2
a
=
=
[3
=
=
=
—
—
.

: azuense
Trisetum gracile E. Four. = Cr, irazuense
Trisetum hallii етп. = S. interrupta subsp. inter-

rupta

Trisetum humile Louis-Marie = P. humilis

Trisetum interruptum Buckley = S. interrupta subsp. in-
terrupta

Trisetum interruptum E. Fourn. = T. s

Trisetum interruptum UNR: ANKE D hallii (Se dn: ) Hitche.
S. interrupta subsp. interrupta

Trisetum interruptum var. californicum Doai Louis-Marie

= S. interrupta subsp. californica
Trisetun m irazuense (Kuntze) Hitche.
orres = P. pringlei

obtusa
artha-go las P М. Peterson & Finot
Trisetum mexicanum (Swi ag an) S. D. Koch = T. viride

Trisetum nivosum E. E = T. spicatum

е

оге, = 1

^ viride
Ше

Trisetum pringlei (Se sane ех Hel Hitche.

Trisetum rosei Scribn

tenerum una ibn & Мег, = T.r

Trisetum rosei fo. tenerum (Sc ibn: & Mer “IT. " Louis. Marie

Trisetum rosel var.

nuns SC 1 0 An Hitche. = T. не
Trisetum scab T. irazue
Trisetum spellenl 1105 I 9 Finot & n M. Peterson
Trisetum spicatum (L.) K. Richt.
i spicatum subsp. lene var.
Hultén = T. barbatipaleu
Trisetum ангор subsp. 1 (Kunth) Hultén = Т.
atum
бш spicatum var. barbatipaleum Hultén =
batipaleum
Trisetum spicatum var. barbatipaleum Hultén ex Veldkamp
I. barbatipaleum
Trisetum spicatum var. nivosum (К.
T. spicatum
Trisetum subspicatum (L.) P. Beauv. = T. spicatum
Trisetum tolucense iene) Kunth = T. spicatum
Trisetum tonduzii Hit
Trisetum viride (Kunth) Kunth
Trisetum virletii E. Fourn.

rivalve Sodiro =

barbatipaleum

T. bar-

Fourn.) Louis-Marie =

REVISION OF METASTELMA
(APOCYNACEAE-
ASCLEPIADOIDEAE) IN
SOUTHWESTERN NORTH
AMERICA AND CENTRAL
AMERICA!

Sigrid Liede? and Ulrich Meve?

ABSTRACT

The revision of Metastelma (Apocynaceae—Asclepiadoideae) in southwestern North America and Central America

(excluding the Caribbe

var. кш and M. schlechtendalii y v" arenicola,
rank (M. arizonicum кү chiapense and M
var.
rank. Four
infimicola as synon
to M. schaffi

a
(oe anc

new sv 'e recogn

o M. schaffneri. The morphology of th

an) is based on field observations and study of
ognized (two of these split into two subspecific units, two into three subspecific units). Two new taxa,
are described.
J. californicum subsp. lanceolatum) and two to ma rank (M. harbigerum
Sd var. trichophyllum). One
ed: Ditassa mexicana as synonym to M
ym to M. шал, М. macropodum as synonym to М. palmeri, 2
North and Central American species of |

f herbarium specimens. Sixteen species are rc
M. barbigerum

Two former species are specific
taxon (M. илеп) is raised from varietal to
californio E subsp. lanceolatum, M.

T. multiflorum as synonym
касера as well as habitats.

spec ies

distribution, and phenology, are desc ribed. In addition to the taxonomic descriptions, Кол: and distribution maps
jd f

are presented for each specie

ey words:

Apocynaceae, КЕНТ Ө Central America,

Vetastelma, North America.

Metastelma R. Br. is an entirely American genus
of Apocynaceae—Asclepiadoideae, with a distribu-
tion ranging from northern Argentina as far north
as Texas. Its center of diversity lies in the Carib-
bean (these taxa are not considered herein). No re-
liable estimates on the number of species are avail-
able, because the concept of the genus has been
subject to unusually large changes (see below). The
number of published names stands at ca. 190—1he
number of species is probably around 70, with 16
found in southwestern North America and Central
America (as detailed here), ca. 30 in the Caribbean
(including eastern North America), and 20-25 in
South America (Liede, unpublished observations).

Within the Asclepiadoideae, Metastelma belongs
to the Asclepiadeae, the only tribe of Asclepiadoi-
deae possessing pendent pollinia (Liede & Albers,
1994). The subtribal delimitation of the large tribe
Asclepiadeae (ca. 100 genera, Liede & Albers.
1994) has been subject to much debate. In the first

subtribal classification for the tribe, which was
based solely on corona characters, Schumann

(1895) placed Metastelma with its gynostegial. but

purely staminal corona in the Asclepiadinae. He

distinguished /rmischia Schltdl. because of its
seemingly corolline corona and placed it in the

Liede (1997), in
define more naturally delimited subtribes. placed
Metastelma (including Irmischia) in the Metastel-
matinae. after Kunze's (1997) study of floral mor-
phology had supported its exclusion from Asclepi-
adinae. 1997)
constituted a large subtribe with members in bath
hemispheres. Recent molecular work.

Tauber. 2000. 2002: Rapini et al..
in prep.) has shown that the New World mem-
(1997)

the. Metastelmatinae s.

Glossonematinae. an attempt to

etastelmatinae sensu Liede (

al..

bers of the Metastelmatinae sensu Liede
form a clade of their own.

in close relationship to the two other subtribes

st
restricted to the New World, Oxypetalinae and Gon-
2003). Ortho-

forms a sub-

olobinae (Liede, 1997: Карт et al.
sia, often confused with Metastelma,
tribe of its own together with Jobinia E. Fourn. and
some former “Cynanchum” species (Liede et al..
prep.). Within the Metastelmatinae

and species delimitation is still difficult, mainly

st

. genus

and WIS f

! First M. p b thank the directors p correspondents of A. ARIZ, B. К,
TEX. the loan of specimens and the

MO, NY. P. , UPS, US,
We г

pleasant companion in the field and very helpful with the

? Department of Systematic Botany, University of Bayre uth, 95440 Bayreuth, (

ulrich.meve@uni-bayreuth.de.

ilso hank M. К (Washington State University) or the «

ANN. MISSOURI Bor.

FR. GH, HAL, HBG, K. LL. M.
‘ir patience in waiting for their return.
апу return of two types. Jim Conrad has been a
artw

зегтапу. sigrid.liede@uni-bayreuth.de:

GARD. 91: 31-86. 2004.

Annals of the
Missouri Botanical Garden

due to the extremely diverse, but poorly known
South American species. In South America, the

species attribution between the florally very similar

genera Metastelma and Ditassa is purely formal.
placing species with a simple staminal corona in
Metastelma, those with a double staminal corona in
Ditassa. It is yet unknown whether reduction of the
inner corona lobe has given rise to “Metastelma”

species that need to be included in Ditassa, and it
is also unknown whether Ditassa-type flowers have
arisen independently more than once from Metas-
telma-type flowers by doubling of corona lobes. In
South America, Rapini (2001) recently suggested
transferring two Metastelma species (M. hemipogo-
nioides Malme and M. hatschbachii Fontella &
Marquete) to Hemipogon E. Fourn., a genus previ-
ously defined by a characteristic erect, slender hab-
it with pendulous flowers, and the absence of a co-
rona (Fournier, 1885). The two species combine the
typical habit of Hemipogon with the corona struc-
ture of Metastelma, suggesting a close relationship
between the two genera.

In Central America (and the Caribbean) in con-
trast, delimitation of Metastelma is by far less com-
plex, even though the unfortunate inclusion of almost
every small American asclepiad with twining habit
and pendulous pollinia in Cynanchum by Woodson
(1941) has led to considerable confusion. Prior to
this (Schlechter, 1899), members of Orthosia Kunth
have been confused with Metastelma even though
they are clearly separable by a combination of a
much more regular branching pattern, adaxially gla-
brous corolla lobes, and an annular corona.

Metastelma has never been revised over a larger
geographical scale. This revision deals with all of

mainland Central America, extending north to the

southwestern United States, the northern distribu-
tional limit of the genus, and south to the Panama
Canal, including the former Canal Zone. It is based
on field observations in the U.S.A.. Mexico, and
Guatemala, and on study of more than 400 herbar-
ium collections from the U.S.A.. Mexico, and Central
America. Previous records of Metastelma are dis-
persed in various floral treatments of different geo-
graphical scope and, in part, of considerable age (see
below). Nevertheless, these records give a good re-
flection of species diversity throughout Central
America. The highest diversity is found in the Son-
oran desert, where Fishbein (1998) listed seven spe-
To the north. di-
(1994) listed two
species for Arizona, and Shinners (1964) listed two

cies for the Río Mayo area alone.
versity declines rapidly. Sundell

for Texas. To the south, diversity declines as well.

Wiggins (1980) listed two species for Baja Califor-

nia. Amazingly, two species are also listed for the

small island of Socorro (Levin & Moran, 1989) (all
hidden under “Cynanchum”), suggesting a consid-
erable capacity for long-distance dispersal. For Mex-
ico as a whole, Standley (1924) listed 14 species.
Further south, species diversity remains low with
five species listed for Guatemala, one each for Belize
Standley & Record, 1936) and Honduras (Standley,
1938a), two for El Salvador (Standley, 1925) (all hid-
den under “Cynanchum”). Two records are listed for
Costa Rica (Standley, 1938b), but one of them, M.
filisepalum, was only attributed to Metastelma with a

pan

question mark and is now excluded from the genus
(see excluded species). For Nicaragua, Stevens
2001) listed three taxa, M. trichophyllum (M. schle-
chtendalii var. trichophyllum) and two MER a

p

species. Species A is identified here as M. schle-
chtendalii var. schlechtendalii, in which the attach-
ment of the corona along the stipe is quite variable,
and species B is identified as M. pedunculare. For
Panama only one species is reported (D'Arey, 1987),
again under “Cynanchum.”

The genus is taxonomically difficult not only be-
cause of its minute flowers, but also because 5 of
the 15 species recognized here form widespread
and variable complexes, the most extensive being
M. barbigerum and M. schlechtendalii. This fact is
reflected by the large number of subspecific units:
subspecies for geographically well-separated taxa
distinguishable by at least one distinct morpholog-
ical character, and varieties for geographically less
clear-cut taxa, distinguishable on the basis of a
weaker morphological character, such as the indu-
mentum. Like the other large American Metastel-
matinae genera, Metastelma is а comparatively
young genus still in the process of speciation and
radiation (Liede et al., in prep

Apart from these widespread complexes, several
species are more or less narrow endemics, most of
the
degree of endemism in Metastelma has been over-

these occurring in northern Mexico. However,

estimated, because several species described

narrow endemics (е... M. macropoda, M. sepicola)
were found to be indistinguishable from species de-
scribed from another area during the present study.
One species,
tical to М.

underlining the close relationship of the Panaman-

M. infimicola from Panama, is iden-
eliasianum described from Colombia.

ian flora with the Colombian one.
Finally. a handful of specimens exist that are ei-
ther

closely related species or deviate considerably from

found far off the distribution area of the most

the most closely related species. These specimens

are discussed in the text under the most closely

related taxon. but until more material becomes

available, it seems premature to describe new spe-

Volume 91, Number 1
2004

Liede & Meve 33
Revision of Metastelma

cies based on what is probably an aberrant speci-
men. The material studied points to a considerable
potential for long-distance dispersal, hybridization.
and introgression, possibly resulting occasionally in
atypical plants or typical plants in unexpected
places.

It is difficult to propose a hypothesis about the
relationships of the species studied, so only a few
obvious relationships will be mentioned. Metastel-
ma barbigerum, M. schaffneri, and M. schlechten-
dalii form a complex in which some specimens
show considerable reticulation of characters. Me-
tastelma minutiflorum and M. latifolium probably
are vicariant species with coastal and inland pref-
erences, respectively. Metastelma mexicanum
shows some affinities to М. arizonicum in gynoste-
gium structure.

TAXONOMIC HISTORY
Robert
Brown (1810), is based on M. parviflorum, and ini-

The genus Metastelma, established by
tially included only that species. During the next
130 years numerous species were added from all
over the Americas, most of them corresponding to
the current concept of the genus. In the Caribbean
Schlechter (1899) included Amphistelma Griseb.
and Orthosia Metastelma, but in Central and
South America, Orthosia remained distinct. Wood-
son (1941) sank all North American Asclepiadeae
into only eight genera, Asclepias L., Blepharodon
Decne.. Cynanchum L., Fischeria DC., Gonolobus
Michx.. Matelea Aubl., Oxypetalum R. Br., and
Sarcostemma R. Br. While Woodson’s (1941) con-
cept was useful for the fast naming of the many
asclepiads emerging during expeditions to Central
South
careful

readily
that
some of the enlarged genera are highly artificial—

and America, and was therefore

adopted, re-examination has shown
in particular Sarcostemma (Liede, 1996a: Liede &
Täuber, 2000) and Cynanchum (Liede & Täuber,
2002; Liede & Kunze, 2002). For Metastelma,
Woodson (1941) stated that he did not know the
genus well enough to carry out the numerous nec-
essary name changes, a task readily carried out in
the course of the various floras published after
1941 (see above). Stevens (1988) reverted to con-
sidering Metastelma as a distinct genus, though
without arguing his case in detail. Like Schlechter
(1899), Stevens (1988) did not consider Orthosia
Metastelma.
ments published in the area after 1988 (Fishbein,
998; Levin & Moran, 1989) follow this usage.
Liede (1997) argued for a distinct genus Orthosia

distinct from The few floristic treat-

for morphological reasons, but did not propose any

formal transfers. Stevens (2001) was the first to re-
establish Orthosia in a flora treatment. Molecular
results based on cpDNA (Liede & Täuber, 2002)
are supporting Metastelma and Orthosia as distinct
genera independent of Cynanchum.

MORPHOLOGY OF THE SOUTHWESTERN NORTH
AMERICAN AND CENTRAL AMERICAN SPECIES OF
METASTELMA

HABIT AND SHOOTS

All Metastelma species are slender twiners that
may extend over several cubic meters, spreading
over bushes and small trees. As far as known, all
species possess a stout woody rootstock, from which
several basally often slightly woody main shoots
originate. In contrast to the often ladder-like
branching pattern of Orthosia, where both leaf axils
sprout a side branch, branching in Metastelma is
highly irregular, and side branches sprout from one
leaf axil only. Shoots may be glabrous, glabrescent.
or pubescent, and the trichomes can occur over the
entire shoot, along two lines, or along a single line.
the position of which changes at every node. Tri-
chomes on all vegetative parts are simple, multi-
cellular. and smooth. Indumentum terminology fol-
lows Hewson (1988) throughout.

LEAVES

The leaves are always decussate; the blades are
usually ovate to elliptic, more rarely obovate or lin-
ear. They bear one to three small glandular organs.
colleters (e.g.. Thomas & Dave, 1991) directly at
the base of the adaxial side of the blade at the
transition point between petiole and midrib. Leaves
can be glabrous or pubescent. Most frequently. the
midrib on the adaxial side of the blade is rather
densely covered with trichomes, the margin is cil-

iate. while the adaxial leaf blade is glabrous.

INFLORESCENCES

A single. always extra-axillary inflorescence is
borne at each node of the 5 part of the
shoot. The inflorescences are 2- to 12-flowered, and
in most cases sciadioidal C E We-
berling, 1989) or only slightly cymose. Only Me-
tastelma pedunculare has a distinctly cymose inflo-
rescence, usually with a single dichasium at the
base. Metastelma pedunculare is also the only spe-
cies in which the peduncles regularly exceed 1 em
in length.

Flowers. The flowers, which are always borne
on a pedicel to 5 mm long. аге 5-partite as char-
acteristic for the Asclepiadoideae. They are usually

Annals of the
Missouri Botanical Garden

nectariferous, but, as far as known, unscented, ex-
cept for M. stenomeres and M. schlechtendalii var.
schlechtendalii, for which a sweet to very sweet
scent is reported (Schipp 674 for M. stenomeres;
Davidse & Brant 32667, Saunders 740 for M. schle-
chtendalit). They are generally very small (corolla
length not exceeding 4.5 mm), and some (M. cu-
neatum, M. latifolium, M. minutiflorum) tiny (co-
rolla length not exceeding 2 mm).
prising display is created by the simultaneous

rather sur-

opening of many flowers per inflorescence and
many inflorescences. In general, the flowers are ei-
ther star-shaped (e.g.. M. barbigerum), or campan-
ulate (M. arizonicum), or almost tubular (M. sten-
The calyx is basally fused, with the lobes
usually less than 1
and pronouncedly acute in M. arizonicum and M.

omeres).
1.5 mm long, but to 3 mm long

mexicanum.

Corolla. The corolla is white, cream, yellowish,
brownish, or greenish abaxially, but always white
to cream adaxially. Characteristic for Metastelma
sometimes

densely indumented,

bearded adaxial sides of the corolla lobes. Several

are the usually

different types of simple trichomes can be distin-
guished. Smooth, hispid, downwardly directed tri-
chomes are found just above the tube in the center
of the corolla lobe in most species (Fig. 1c). Long,
slightly verrucose and soft trichomes may form the
"beard" at the tip of the corolla lobes, e.g., M. bar-
bigerum var. barbigerum and M. pringlei (Fig. 14,
e). Shorter, more strongly verrucose trichomes are
found in the apical and marginal parts of corolla
lobes of taxa without a distinct "beard." e.g., M.
barbigerum var. liesnerianum (Fig. Le).

Corona. The corona is of gynostegial origin, but
can occasionally be fused basally to the corolla (M.
parviflorum, M. mexicanum). In contrast to Ortho-
sta, in which the corona is fused for at least one
third of its length, it consists of free staminal parts
only (Kunze, 1997).
and variation between species comes about by var-

The corona is always white,

iable length in relation to gynostegium length,
shape, and fleshiness, e.g.. in M. barbigerum, the
corona is about as long as the gynostegium (Fig.
la), while it is considerably longer with its parts

connivent over it in M. pringlei (Fig. 1b). Point and
angle of attachment of the lobes are further distin-
guishing characters: in both M. barbigerum var.
barbigerum and M. pringlei the corona lobes form
a distinct hook at the point of attachment (Fig. la,
b). while this hook is much less pronounced, e.g..
in the other two varieties of M. barbigerum as well
as in M. schlechtendalii.

Gynostegium. The gynostegium can be either
sessile, or elevated by a stalk (Fig. la, b). In gen-
eral asclepiad terminology, a stipe. a feature occa-
sionally found in Cynanchum, is a stalk elevating
the gynostegium, but not the corona, and a column,
typical for the Asclepiadinae, is a stalk elevating
both the gynostegium and the corona. In Metastel-
ma, the corona can be attached to the base of the
stalk (e.g.. M. parviflorum), along the stalk (e.g., M.
eliasianum, М. barbigerum, М. arizonicum), or di-
rectly underneath the gynostegium (e.g., М. pedun-
culare, М. stenomeres). While the terms “stipe” and
“column” have been used in the descriptions ac-
cording to their definitions, all intermediate states
exist, so that the distinction is purely formal. The
outline of the gynostegium is a useful character in
species identification, especially for the large and
variable M. barbigerum and M. schlechtendalii
complexes. Metastelma barbigerum always has a
conical gynostegium with inclined anthers (Fig. 1а),
while M. schlechtendalii always displays a more or
less cubical gynostegium with erect anthers. In the
Yucatán, this character
short-stiped forms of M. schlechtendalii from М.

distinguishes even the

barbigerum var. veracruzense and variety liesnerian-
um, in which the hook-shaped corona attachment
and the corolla “beard” easily identifying the typ-
ical variety are often less well developed. The guide
rail, formed by the anther wings of two adjacent
anthers is as long as the anther proper, except for
M. schaffneri, where it is slightly shorter. It consists
of an outer and an inner ridge, with the inner ridge
shorter than the outer one and strongly curved (Fig.
1f). Pollinaria are minute and therefore difficult to
use for identification, even though the shape of cor-
puscula, caudicles, and pollinia are species-specif-
ic. The lower part of the style-head possesses a

Figure 1.
ew; two petals removed. —b.

neriani um,

<

up}
d. Metastelma pringlei, simple, slightly verrucose trichomes on upper regions of corolla lobe surface

SEM studies of flowers and flower details. —
Metastelma pringlei. 5 with corona.
yer regions of corolla lobe surface with smooth trichomes (ce in r) and verrucose trichomes (margins), —

—

. Metastelma num var. nic 0 in lateral
—c. Metastelma barbigerum хат. lies-

. Metastelma

barbigerum var. barbigerum, detail 10 verrucose hair from median region of adaxial corolla lobe siriane 'e. _( Metastelma

'arbige rum var. barbigerum, detail of gynostegium s

"а and опе pollinium with е one anther removed.

ede & Conrad 3242.

showing one pu with dis

tal and proximal ridge (arrow) of anther
: Liede & Conrad 2610; b. d: Liede & Meve 2501;

Volume 91, Number 1 Liede & Meve
Revision of Metastelma

Yor

\ d
AUF UM
$ NN. p م‎
*

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Annals of the
Missouri Botanical Garden

knob above the corpusculum and the upper part of

the style-head is flat to conical in most cases. Only
М. mexicanum can be easily recognized by its ob-
infundibuliform style-head.

icles and seeds. One follicle per flower is
generally developed. A compitum (Kunze, 1991) is
thus absent. Follicles are slenderly obclavate to fu-
siform in shape, with a thin pericarp and without
wings or other ornaments. Each follicle contains 10
to 20 seeds in an imbricate arrangement on the
placenta. Seeds are ovate, oblong, or pyriform,
winged or wingless, light to dark brown, glabrous
or papillate, smooth, with longitudinal ridges or tu-
berculate, but no species with seed trichomes has
been found.

CHROMOSOME NUMBERS

Of the species in western North and Central
America, only Metastelma barbigerum var. barbi-
gerum has been counted with 2n 2 (Albers et
al., 1990, as Matelea reticulata (Gray) Woodson),
the chromosome number found in more than 90%

of all Asclepiadoideae (Albers & Meve, 2001).

HABITATS, DISTRIBUTION, PHENOLOGY, AND USES

Most Central American Metastelma species dis-
play a rather wide ecological amplitude and occur
on various soils and in numerous vegetation types.
Metastelma arizonicum subsp. arizonicum is a low-
land desert scrub species, and M. californicum
subsp. californicum occupies even drier habitats.
Both taxa have a South or Central Mexican sister
taxon living at higher altitudes and in forest habitats,
open pine forests for M. arizonicum subsp. chiapense
and tropical deciduous forests for M. californicum
subsp. lanceolatum. Of the remaining Sonoran spe-
cies, M. cuneatum and M. minutiflorum are restrict-
ed to the lowlands (to 200 m), where they inhabit
thornscrub communities. Metastelma latifolium and
M. mexicanum prefer altitudes above 200 m (to 1500
m) and live in open forest communities.

In Texas, Metastelma barbigerum var. barbigerum
is commonly found in lowland areas (below 500 m),
while M. palmeri prefers higher altitudes (above
500 m). In Mexico, though, M. barbigerum var. bar-
bigerum is also found at higher altitudes to 2300
m, while the other two varieties are strictly lowland
plants of sand dunes, rivers, and disturbed habitats.
A similar difference in altitudinal preference char-
acterizes the three subspecies of M. schlechtendalii.
The typical variety is salt tolerant and occurs main-
ly in open or disturbed locations close to the sea,
but is occasionally found as high as 2000 m in

Guatemala. Morphologically extremely similar is

the strictly coastal disjunct variety arenicola. Va-
riety trichophyllum, easily recognized by its densely
hispid leaves and more floriferous inflorescences,
in contrast, prefers altitudes over 750 m and open
forests. Other lowland species are M. stenomeres, a
distinctive Belize endemic living in open pine for-
ests, and М. eliasianum, extending from Panama to
the west coast of South America (Colombia). The
remaining four species, M. longicoronatum, M. pe-
dunculare, M. pringlei, and M. schaffneri, occur
regularly at altitudes between 1000 and 2500 m,
although some specimens have been found as low
as 500 m or as high as 2800 m. No Metastelma,
however, was found above 3000 m. The latter four
species, except for M. pedunculare, which has a
weedy tendency, live in open forest habitats.

Very little is known about the reproductive and
pollination biology in any species of the genus.
Liede (unpublished) observed a small bee visiting
Metastelma californicum subsp. ca 5 and
Fishbein (Fishbein & McMahon 2769
observed bees, wasps, and flies TEN Sp., Halicti-
dae, Sphecidae, and Diptera) on the same species.
The host-plant ages by Markku Savela, (http://

et. 0 MEL) 577 1.251.

ww.nic.fun
m. к lists Matasielma as probable host for "A
butterfly Anetia thirza insignis (Salvin, 1869) (Nym-
phalidae) in Panama and Costa Rica. Fruits have
been observed in all but three species (M. latifol-
ium, M. longicoronatum, M. stenomeres), but not to
the extent suggesting that Metastelma belongs to
the extremely rare asclepiads capable of self-fertil-
ization, as e.g., Tylophora hirsuta Wight (Chatur-
vedi, 1988) and Vincetoxicum nigrum (L.) Moench
(Lumer & Yost, 1995). The phenology data pre-
sented in the species descriptions are based on col-
lections of these species over their entire range (see
Appendices 1, 2; an index to scientific names is
provided in Appendix 3). While most species show
a distinct peak of flowering at a single locality, this
peak may shift with changing geographical param-
eters. Also, most species continue to produce a few
flowers after their peak flowering time is long past.

Metastelma is not generally noted among the rec-
ognized useful plants. Morton (1981: 692) noted,
"Indians of Yucatán boil the root and repeatedly
rinse the mouth with the decoction to heal canker
sores. They warn that the decoction must not be

swallowed."

TAXONOMY

Metastelma R. Br, Asclepiadeae: 41. 1810.
TYPE: Metastelma parviflorum (Swartz) R. Br.
[= Cynanchum parviflorum Swartz].

Volume 91, Number 1
2004

Liede & Meve 37
Revision of Metastelma

Imp. Naturalistes Moscou
Acrocoryne caribaea Turcz.
basset Bartlett, Arts 44: 631.
909. TYPE: Basis mexicanum (Brandegee)
En [7 Melinia n mexicana Brandegee |]. lectotype,
designated here.
Devas Schltr., in Urban, Symb. Апи.
^E: Dec 5 broadw ayi Schltr.

qu Turez.. Bull. Soc.
5(2): 316. 1852. TYPE:

A Acad.

1: 264. 1899.

* — FI. mi 149. 1913. Type: Epicion ba-
hamense Vie Small (Metastelma | bahamense
Gr

Irmisc hia “Sch Idl., Linnaea 19: 738. 1847. TYPE: /rmis-

chia floribunda Schldl.

Meresaldia Bullock, Kew Bull. 19: 203. 1965. Esmeraldia
. Fo

Qc
85
=]
o
~]
ج‎
»
3
R=.
Sy?
A,
=
—
-
E
5 57

1862 (Orchidaceae).
Fourn.) Bullock = Esmeraldia stricta E.

Stelmation E. Fourn., in Martius, Fl. Bras. 604): 226.
1885. TYPE: Stelmation myrtifolium (Decne.) E.
Fourn. [= Metastelma myrtifolium Decne. ].

to 400 em high,

subterranean

Plants small, slender twiners.

richly irregularly branched; organs
constituting a woody rootstock: shoots herbaceous,
basally often slightly woody or corky, pubescent,
glabrescent or glabrous; latex white to ivory; pseu-
dostipules (extremely reduced short shoots with a
pair of smaller and sometimes differently shaped
leaves) absent. Leaves opposite, petiolate, with 0 to
3 colleters at blade base: blades herbaceous. Inflo-
rescences usually one per node, extra-axillary, 2- to
12-flowered, bostrychoid or sciadioidal, peduncu-
late to sessile; floral bracts present, triangular or
ovate. Floral buds elongated-conical, conical, ovoid
or cylindrical; calyx basally fused, campanulate,
lobes ovate, acute to acuminate; corolla rotate to
campanulate to almost tubular, 1.5-4.5 mm long,
abaxially white, cream, yellow, green, or brown,
glabrous, adaxially white, densely covered with
verrucose and smooth trichomes, arranged in spe-
cies-specific patterns; gynostegial corona of free

staminal lobes, white, glabrous; lobes simple. Gy-
nostegium sessile or atop a stipe or a column; an-
ther wings consisting of distal and proximal ridge.
proximal ridge short, curved; connective appendages
present, ovate or triangular; pollinarium with two
pollinia per pollinarium, (sub)apically attached to
the caudicles, pendulous, not possessing a germi-
nation pore; upper part of the style-head depressed-
conical to conical, rarely flat or elongated-conical.
Follicles one, occasionally two per flower, 25—80
mm long, obclavate or fusiform, terete or obtusely
deltate in cross section, apically beaked, wingless,
slightly longitudinally grooved, usually glabrous,
with thin pericarp; seeds 4-7 mm long, brown,
winged or wingless, glabrous or papillose, smooth
or with longitudinal ridges or tuberculate, without
trichomes, comose.

Chromosome number. 2n = 22 (Metastelma
barbigerum var. barbigerum, Albers et al. (1990).
as Matelea reticulata (Gray) Woodson).

Basistelma was created by Bartlett (1909) to ac-
commodate two species, B. angustifolium (Torr.)
Bartlett and В. mexicanum (Brandegee) Bartlett,
that are at first glance ill fitted in Metastelma be-
cause of their long, conspicuous style-head. Fish-
bein and Levin (1997) correctly included Basistel-
ma in Metastelma, and recognized the two former
Basistelma species as identical. As the basionym
of B. angustifolium, Metastelma angustifolium
Torr., is a homonym of Metastelma angustifolium
Turez. (a taxon belonging to the genus Orthosia)
and thus not a name available in Metastelma, Fish-
bein and Levin (1997) assigned the name Metas-
telma mexicanum (Brandegee) Fishbein & Levin to
this species. Under these circumstances, it is log-
ical to select Basistelma mexicanum as the lecto-
type of Basistelma, an action not carried out by

Fishbein and Levin (1997).

KEY TO THE SPECIES OF METASTELMA IN THE SOUTHWESTERN U.S.A. AND CENTRAL AMERICA*

la. Gynostegium sessile or almos
2

so.
Flowers tiny; corolla lobes not longer than ca. 2 mm (northern Pacific slope of Mexico only).

3a. Corolla lobes puberulent with very жой trichomes (< 0.1 mm long); corona distinctly 15 555 nar,
at les cu

ast basally as broad as the ant

neatum

3b. C х Па lobes densely covered with p trichomes (> 0.1 mm long); corona lobes + ad

distingüy smaller than the бү 5

o.
e
=<
Ф
|
—
3
O
@
-$
e
©
<
se

ho

5b. Base af stained corona lobes at the base broader than the ps plants of c
3b. M

Mexico
Ib. Gynostegium with a distinct stipe.

a
p apiculate, shoots with one line of trichomes, — with a pedun

2.4
. Flowers larger; ELA р at least 2.5 mm SE
5a. Base of staminal corona lobes жй а than the anthers; plants of northern Мех
За. М.

enderly lanceolate, shoots with two lines of trichomes, inflorescences
d co 9. M.

i tui

6. M. LI.
3. M. californicum

1

. californicum p^ ай eto eb aii
entral and sout
. californicum subsp. а

р
Stipe as long as ће gynostegium or shorter than it.

Annals of the
Missouri Botanical Garden

Та. Corona distinctly shorter than the gynostegium; anther appendages about twice as long as the
anthers, erect; style-head with a pronounced appendage; corolla lobes apically with very short (<
0.05 mm long) verrucose trichomes (giving a papillose appearance) and a tuft of smooth, stiff
trichomes at the base of each corolla lob. 8. M. mexicanum

Tb. Corona as long as or longer than the gynostegium; anther appendages not longer than the anthers,
inflexed; style-head without a pronounced 5 corolla lobes apically with distinct tri-
chomes (at least 0.1 mm long) and smooth trichomes, if present, not 3 to a small tuft.

8a. Corona ca. 1.5 mm long, about twice as long as 7 gynostegium, including stipe, concealing
the gynostegium 00 00 12. M. мй

8b. Corona shorter than 1.5 mm, 1.5 times as long as the gy noste; gium (incl. stipe) or less, not
concealing the conical gynostegium.
9a. din distinctly lanceolate, suddenly broadening at the base, ce an almos
istate shape o . M. a
9b. Corona never sudde nly broade ning at the base to produce e a hastate P 1ape.

Ja. Corona attached along the stipe, lobes subulate and bases hardly broader than
apex or slenderly ovate to lanceolate, with or г without a long extended tip, often
attached to the stipe with a pronounced ho

la. Corona attached to the stipe with a oe ‘ed hook, lobes longer than 1
mm and style-head longer than 0.5 mm.
12а. Stems and pedicels with a eh line of rec trichomes; calyx
with a few sparse trichomes; leaves less than 3 mm wide: corolla
lobes oblong or ovate, but not apically sudde nly narrowing; trichomes
of the EA side of the corolla lobes apically not —— longer
than laterally
13

2

V. arizonicum
Stems basally often corky. € veins with tric homes; calyx lobes
ery slenderly ovate, almost as lon g as the corolla lobes, but at
ln reac hing half of corolla 7 ah corolla lobes adaxially lat-
erally and apically with long (0.2-0.3 mm), distantly verrucose
tric homes; plants of the ала U.S.A. and northern Mex-
x arizonicum subsp. arizonicum
13b. Stems basally never corky, lod ins glabrous, calyx lobe
ovate, not very slender and not reac cra half of corolla le 8
corolla lobes adaxially apically and laterally with short (ca. 0.1
mm), strongly verrucose trichomes; Mee of southern Mexico,
Guatemala, Honduras lb. M. arizonicum subsp. chiapense
12b. Stems, нет els, and calyx glabrous, corolla lobes ovate to lanceolate,
en apically rather abruy Aly narrowing; trichomes of wed adaxial side
of the corolla lobes apic ally distinctly iro than laterally

ко

М. 5 var. een
11b. orona + - flatly attac died inda 'rneath the gynostegium, either lobes shorter
ian 1 mm or style- head shorter than 0.5 mm, or both.

>

Ma. Pedicels glabrous; stems glabrous or with, a single line of trichomes,
calyx with a few isolated trichomes on b tube —

>:

›. М. barbigerum var. liesnerianum
14b. Pedicels dipai ly covered with tric hones stems always with a
occasionally very broad line of trichomes; calyx with trichomes с
- 2с. barbigerum var. veracruzense
10b. Corona attac hed dim ctly ат the empiece: Ibis ovate to triangular,
ays without a long extended tip, never attached to the stipe with a pronounced
hook.
15a. Leaves, at least those of flowering branches, mostly linear or lanceolate,
rarely ovate; corona lobes not distinctly flat, oblong, considerably exceeding
the fla tly cylindrical gynostegium .. М. Sin dd
eaves normally ovate; corona lobes dis stinctly flat and muc h broade ra
the base than at the apex, barely exceeding the slightly conical gy ай ка

15b.

gium.

l6a. Trichomes of the adaxial side of the corolla к! and laterally of
equal length and fairly short (0.1—0.15 mm); leaves na rrowly ovate,
on жакын ranches not exceeding 15 mm bu corolla usually less
than 2.5 mm (rarely to 3 mm) long 10. M. palmeri

16b. Tric homes of the adaxial side of the corolla apically slightly май
E terally (to 0.2 mm); leaves ovate, on cli: — s to 25
nm теа corolla to 4 mm long
Ob. Stipe distinctly longer than the gynostegium.
7a. Corolla fused at least for a quarter of total length.
8a. Corona attached to the stipe immediately below gynostegium.
Corona almost twice as long as the gynostegium without stipe; style-head conical;

— BED = e turneri

—
8

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

dioidal; floral bracts elabrous

eaves slenderly elliptic or геи peduncle 3—

5 mm long: inflorescences scia-
15. M. stenomeres

5.
19b. Corona just exceeding the gynostegium: style- e 1d flat; R es ovate; к ‘le at least

) mm s inflorescences bostrychoid: floral bracts ciliate
Corona not attached immediately below gynostegium.
20a. Ce to stipe: corolla (ооо for less than half of its length, lobes

18b.

4h bi ittachec

M. pedunculare

dense, p Be woolly trichomes: stipe stout, not more than twice as long r as the

ynostegium; plants of C entral and South. America /
20b. c orona attached to the corolla: pones fused for half of its length or more. labe 8

L short pube scence : stipe

stegium: plants of South 5

Corolla Е» ab basally (

17b.

(corona attached кер stipe y E»

M ۹ OEE М. “Тее чыш

ith
ery slender, at least three times as long as the gy-
DEI PL. . parv iflorun т К.
М. schlechte мий

21а. Adaxial leaf surface with evenly spread trichomes; inflorese ences s usually sith more than

"pina pedicels with evenly distributed trichon

21b.

Adaxial le id ud e (except for midrib)

1. sc Wy htendalti var. . trichophyllum

hon tric isha = ‘ences usually with less

than 6 flowers; pedicels with a single line of trichomes or glabrous
22a. Inflorescences distinctly pe fie ulate, peduncles normally more than 4 mm long: ы

acts and sepals ovate: corona exceeding the gynostegium by less than gynosteg
length: style-head fat to slightly поа Да. М. schlechtendalii var. schlec -—
22b. Inflorescences subsessile. pedune Jes less than 4 mm long; floral bracts and sepals

distinctly lanceolate: corona exc 'eeding the gynostegium by as much as or more than

gynostegium length: stvle-head distinc tly реса
1.

* Metastelma E illorum is not treated here in detail. but
is included in the key because it is widespread in the
Caribbean and Soal America, and th
been applied to material of M. schlechtendalii.

e name has often

l. Metastelma arizonicum A. Gray, Proc. Amer.
Acad. Arts 19: 85. 1883. Cynanchum arizon-
icum (A. Gray) Shinners, Sida 1: 365. 1904.
TYPE: U.S.A. Arizona: Pima Co., hills near
Tucson, 22 May 1883, C. G. iur 20 (ho-
lotype. GH not seen). Figures 2a—h,

la. Metastelma arizonicum A. Gray subsp. ar-
izonicum

Metastelma w atsonianum Standl.. Contr. U.S. Natl. Herb.
23: 1175. 1924. Basionym: Metastelma albiflorum 5.
Wat аг, Amer. Acad. Arts 24: 60. 1889,
Meroe аи Griseb., Fl. Brit. W. Ind.:
TYPE: Mexico diim baec E. Pa He
"e diste GH not seen; isotypes. NY—21).

Sonore

Plants ascending, 80-250 cm high: shoots pe-
rennial. basally corky, isolatedly to sparsely cov-
ered along a single line with recurved trichomes,
ca. 250-300 um long; internodes 1—4 cm long, ca.
| mm diam. Leaves with petioles 1-2 mm long. with
or 2 colleters at blade base; blades 10-20 X 1.5-
3 mm, elliptic to ovate, basally rounded to cuneate,
apically acute to acuminate, marginally straight or
revolute (when dry). adaxially and abaxially gla-
brous, but sparsely covered on the midvein and

200-250 um

long. Inflorescences always one per node, l- to 4-

margins with recurved trichomes,

flowered, 1 to 4 flowers open synchronously, scia-
dioidal, subsessile: floral bracts 1-1.5 X 0.20.5

). M. SOS d var. eo

mm at the base, deltoid, slightly papillose and with
trichomes on the surface; pedicels 1-2 mm long.
sparsely covered over the entire surface with re-
curved trichomes, 200-250 um long. Floral buds
with im-

2.5-3 mm long, 1-1.5 mm diam.. ovoid.

bricate aestivation; calyx basally fused. campanu-
late, abaxially vaguely glandular. with a few sparse
0.3—0.5 mm,
slenderly ovate, apically acute; corolla campanu-
late, 2.5—4 mm long.

adaxially with distantly verrucose trichomes, 200—

trichomes: calyx lobes 2-2.5 very

white, abaxially glabrous,

300 pum long, on the apical and on the lateral parts
f the lobes and with downward-directed, hispid
trichomes, 300-500 um long, on central part of the
lobes at the mouth of the s lobes fused for ca.
%4 of total corolla length, 1 mm wide. patent and

ecurved, apically acute: hubs corona 1.5-2
mm long. equaling to longer than the gynostegium:
lobes inflexed or apically reflexed. attached at the
base of the stipe with a distinct hook-shaped base.
laminar to solid, subulate. Gynostegium ca. 1.5 mm
high. ca. 0.7 mm diam., on a stipe 0.7 mm long:
anthers about as high as broad, deltoid, abaxially
convex; anther wings ca. 500 um long. extending
along the entire length of the anther, anther wings
of adjacent anthers parallel to each other, in the
same plane as the anther to slightly centrifugal:
1. 250

um wide, triangular, equaling the stamen in width,

~
nA

connective appendages ca. 400 jum long.

erect; pollinarium with corpusculum 150 jum long.
more than twice as long as broad, elliptic: caudicles
80 um long, cylindrical, s-shaped. convex-concave:
pollinia subapically attached to the caudicles, 200—

40 Annals of the
Missouri Botanical Garden

\ Ан S

W | 5

DNE

vy

0.5 mm

0.5 mm

Figure 2. Metastelma arizonic um. m p Metastelma arizonic um subsp. arizonicum. aH Metastelma arizonicum
LO „саре nse. Ha LC

а, a’. . —b, b’. Flower. е, e”. Corolla lobe, ac daxia view. —d'. Corona and gynostegium.
—e, . Pollinarium, —f, Po Style- he de —pg. Follicle. li. Seed. a : Steinmann & Varela 972. g. h: Neese &
тыя 10076. a’: Ghiesbreght 664. b'—(': Lie da & Conrad 2559. Drawn b J. Conrad.

Volume 91, Number 1 Liede & Meve 41
2004 Revision of Metastelma
| ac = — ad i
EN | | | 2;
{4 Р
fo _ oe = — — 35°
— b J
Е | } “умыл |
© Y [tC e | | E f |
‚ 4 ® % Oo B P1
1 т m NENNEN X y |
| ` > | | ) — | —
N Q | | | t Cà “ч JA dae *
4 s } بت‎ = i = | І 2 : = TP 30°
y э „л,
A taal
NI as EN ў |
Mi
= lS НЕ ЧЕ —R '
b^
| К L
A
ө м. рема 55р. arizonicum b M x yi TT G
ч. =; | ca |
A M.arizonicum ssp. chiapense 1” х PO, | eta dn | Y
© М. mexicanum E A E
AE 44 3) 4 =
| — | — — Ne 7 = А A
| КДУ А-А
-120° -115° -110° -105° -100° -95° -90°
Figure 3. Distribution of Metastelma arizonicum and М. mexicanum.

220 um long. 80 um wide. ovate in cross section,
clavate: style-head white, 0.4 mm diam., 0.5 mm
high. upper part 0.2 mm high, shorter than to
equaling the lower part, depressed-conical to con-
ical. Follicles always one per flower, pendulous,
45-65 mm long. 3—4 mm diam., fusiform, terete,
apically strongly beaked, medium to dark brown,
glabrous: seeds ca. 10 per follicle, 5-6 mm long,
2-3 mm wide, pyriform, medium brown, seta and

aseta side tuberculate, marginally with 0.15 mm

wide wing with entire margin: coma 20-30 mm
long.
Phenology. Collected in flower in April, June,

and from August to January; in fruit from March to
May and September to January.

Distribution. | Mexico: Sonora; U.S.A.: Arizona;
mostly on rocky slopes in desert scrub communi-
10-1000 m.

Literature and illustrations.

pl. 18)

ties:

Wiggins (1940: 92,

pia ig pes ns examined. MEXICO. Pape
8.3 rd. of Arizpe on MEX Hwy. 2. J Sep. 19

(fl fr), — 96-27 (ARIZ); Arroyo К | Mentidero, iE :

km S of Alamos, 25 Nov. 1993 (fl, fr), Van Devender et al.
93-1310 (ARIZ); near purs 3 on NE side of
Rio Yaqui hit on S ME 1 . 15 Se )98 (f). Van De-
vender & Reina 98-1152 (ARIZ), y to hus San C “ү
12 Jan. 1965 (fl), Thomas & Felger 11942 (ARIZ): ca. |
mi. N of Bahia San Carlos on rd. to Algodones. 24 Nov.
1963 (fl), Felger 9579 (ARIZ): Bahía Credo E side of
Morro Colorado, 28 Dec. 1966 (fl, fr). Felger 15588
(ARIZ); Bahia de s Pedro, Sep. 1954 (fl, fr), Turner ү
al. 79-261 0 . 5 km E of Bahia San Pedro, 17
er ud prn 84-461 (ARIZ, ie
4 (fl, fr). Van Dev ender &
Van Devender et al. 84- % (ARIZ);
Guaymas 38 ‚ 1965 (fl), y xem & Felger
11785 (ARIZ): achiste about Bahia Topolo-
1 Sep. 1954 (fl. fr). Ld 1 (ARIZ, LL); Cerro
del Viejo SW of Caborca, 9-11 1954 (fl. fr). Gentry
14466 (ARIZ); 23 mi. 5 of hy 26 Sep. 1934 (fl).
Wiggins 7491 (ARIZ): El Baviso, ca. 2.5 km NE of Bahia
San Carlos, 18 Nov. 1984 (fl), Felger & Zamulio 84-490
(ARIZ); Enseñada Chica ca. 23 km N. 39 km W of Guay-
mas, | Oct. 1979 (fl, fr), Burgess 5695 (ARIZ); Ensenada
runde [= Bahia San Pedro]. 11 Nov. 1964 (fl). Russell et
ы oleae m уо, 23 Oct. 1934 (fl).

suajaray, Rio Ma

Gentry 1098 (ARIZ); Guaymas, Palmer 626 (NY); 2 km
E of MEX 15 on e to Microondas Las Av vispas. 21 Sep.
1997 (fl). Reina et al. 96-286 (ARIZ); 1 km E of Los
Camotes, along Los Tanques-Las Chinacas rd.. 18 Aug.

San Bernardo, Rio

1994. Fishbein et al. 1878 (ARIZ):

42

Annals of the
Missouri Botanical Garden

Mayo, 12 Feb, 1935 (fl), Gentry 1298 (ARIZ); Sierra Cip-
riano, 28 Apr. 1991 (fl, fr), Peer dp ш iip arenas
91-33 (ARIZ); Sierra Libre, ca. 2 km E of the tion
with MEX 15, 2 Sep. 1996 (fl), Ботла & е ‚ 972
sup NV): Sierra Seri, Hast : епа, 17 Apr. 1‹ 74 (fl.
Вени et al. 74-15 с S.A. Arizona: |
SU eiie Mis., 8 Oct. МА
Gould et al. 2804 (NY - Babonuiven Mts., Fi
yon, 7 Sep. 1931 (0). Gilman 140 Ща dicis Mts., 19
Oct. 1945 (fl), Goodding 208-45 (NY); 3.5 mi. below Mol-
ino Basin poa Santa Catalina Mts., 18 Apr.
(fl, fr), Keil 432 ): Santa Catalina Mts., 21 Dec.
(fl, fr), Tourney s.n. 155 Sierra Tucson, 26 May 1884 (fr),
Pringle s.n. (NY, topotype): Ventana Park, E of San Mi-
guel, 13 Oct. 1945 (fl. fr). Condding 116- po ак Pinal
Co., Superstition Mts., px ih 206, . 20 mi.
E of Phoenix, 14 Apr. 1981 (A, i Yer 4 кона 10076
(NY). County not EE ge Apr. 1884 (fl, fr), Le Roy s.n.
(NY); Sonora, 15. Aug. 1884 (fl), epa s.n. (NY).

guesl e

2

Ib. Metastelma arizonicum A. Gray subsp.
chiapense (A. Gray) Liede & Meve, comb. et
stat. nov. Basionym: Metastelma chiapense A.

Acad. Arts 21: 397. 1886.
Cynanchum chiapense (A. Gray) Standl &
Steyerm., Publ. Field Mus. Nat. Hist., Bot. Ser.
23: 226. 1947. TYPE: Mexico. Chiapas: 1864—
1870, A. В. Ghiesbreght 664 (holotype, Е (neg.
05966 1)!; isotypes, GH not seen, MO not seen,
NY!). Figures 2a’-f", 3.

Gray, Proc. Amer.

„ 5 S. E Blake, Contr. U.S. Natl. Herb.
19. 2. Cynanchum соШпит (S. F. Blake

—

. ^ я yerm., Publ. Field Mus. Nat. Hist., Bot.
Ser. 23: 226. 19 d TYPE: Guatemala. Pu trail
fom Los Amates to Izabal, 31 May 1919 Blake

7793 (holotype, Us. 989029!; isotypes, С н по! seen,
US not seer

Plants ascending, ca. 50 em high, richly basi-
tonically to irregularly branched. Subterranean or-
gans constituting a woody rootstock; shoots peren-
nial, sparsely covered along a single line with
recurved trichomes, 200-250 um long; internodes
1.5-5.5 em long, 0.5-1 mm diam. Leaves with pet-
ioles 1-2 mm long, with | or 2 colleters at blade
base; blades 15-35 X 1.5-3 mm, linear, elliptic,
or ovate, basally rounded to cuneate, apically acute
to acuminate, adaxially and abaxially glabrous, but
marginally sparsely ciliate. Inflorescences one, oc-
casionally two per node,

3- to 7-flowered, З to 5
flowers open synchronously, sciadioidal, sessile to
subsessile; floral bracts 0.6-1 X 0.3-0.5 mm at the
base, ovate; pedicels 1-3 mm long, sparsely covered
over the entire surface with recurved trichomes,
100-150 jum long. Floral buds 1.8-2.2 mm long,
1-1.5 mm diam., ovoid; calyx basally fused, rotate
to campanulate, abaxially vaguely glandular and
with a few sparse trichomes; calyx lobes 1—1.5 *
ca. 0.5 mm, ovate, apically acute; corolla campan-

ulate, 2-2.5 mm long, abaxially and adaxially
white, abaxially glabrous, adaxially with verrucose
trichomes, ca. 100 um long, on the apical and on
the lateral parts of the lobes and with smooth,
downward-directed trichomes, 300-400 um long,
on the central parts of the lobes; lobes fused for ca.
% of total corolla length, 0.8-1.2 mm wide, erect,
apically recurved, ovate, apically acute; gynostegial
corona 1.2-1.5 mm long, equaling the gynostegium;
lobes slightly inflexed, attached at the base of the
stipe with a distinct hook-shaped base, laminar to
filiform, oblong. with entire margins. Gynostegium
са. 0.8 mm high, ca. | mm diam., on a stipe 0.6
mm long: anthers about as high as broad, deltoid,
abaxially convex; anther wings ca. 300 jum long,
anther wings of adjacent anthers parallel to each
other, centrifugal; connective appendages ca. 400
um long. ca. 300 um wide, ovate, equaling the sta-
men in width, slightly inflexed; pollinarium with
corpusculum 150 jum long, more than twice as long
as broad, elliptic: caudicles 70 um long, cylindri-
cal, slightly s-shaped, convex-concave; pollinia api-
cally to subapically attached to the caudicles, 200—
220 um long, 80 um wide, ovate in cross section,
clavate; style-head white, 0.5 mm diam., 0.5 mm
high, upper part 0.25 mm high, depressed-conical
to conical. Follicles and seeds unknown.
Phenology. Collected in flower in April, May.
July, and from September to November.
Santa Ana; Guate-
mala: Péten; Honduras: Morazán; Mexico: Chiapas:

Distribution. El Salvador:
rocky slopes, very open pine forests; 650-1700 m.

Metastelma arizonicum, M. barbigerum, and M.
pringlei form a group of closely related species.
They share bearded corolla lobes, the conical shape
of the gynostegium, and the protruding anther
wings. Yet, they are relatively easily separated by
the length of the corona lobes (ca. 1.5 mm long,
about twice as long as the gynostegium in M. prin-
glei, shorter than 1.5 mm and at the most 1.5X as
long as the gynostegium in M. arizonicum and M.
barbigerum) and the more slender shape of the gy-
nostegium of M. arizonicum compared to M. bar-
bigerum. Metastelma arizonicum and all varieties of
M. barbigerum except variety veracruzense have dis-
tinctly clavate pollinaria, while those of M. pringlei
are ovoid. In M. arizonicum subsp. arizonicum and
M. pringlei strongly verrucose trichomes on the co-
rolla lobes are absent, while they are present in
subspecies chiapense as well as in M. barbigerum.

Despite the relatively wide distribution gap be-
tween the two subspecies of M. arizonicum (Fig. 3),
the morphological differences between the taxa are
rather inconspicuous, mainly concerning size dif-

Volume 91, Number 1
2004

Liede & Meve 43

Revision of Metastelma

ferences and variation in indumentum density on
leaves and calyx, as well as the presence of strongly
verrucose trichomes on the corolla lobes (present
in subsp. chiapense, absent in subsp. arizonicum).

Additional specimens examined. EL SALVADOR.
Santa Ana: vicin nity of Santa Ana, 28—30 June 1922 (fl).
Standley eee (NY). GUATEMALA. Petén:
about 3 km NWW of village, 18 Oct. 1961 (fl).
3068 (LL). ы. RAS. El Paraíso: Rio Dantas, 5 July
1962 (fl). 1 did ин. Morazan: entre Las Mesas
alme carretera Danlí-Yuscarán.
. 1963 (fl). olaa 13162 ( JL. NY); entre km 11-

arretera Suyapa a La Montañita, 11 Sep. 1963 (fl).
Molina 12851 (NY. ). MEXICO. Chiapas: Cerro del Ocote,
' of Ocozocoautla, ds Oct. 1972 к pa
22 (NY): La Cienega de Leon, 30 km N of Las Cr
30 Nov. 1980 (fr). Breedlove "48083 (MO): Comitán D
Dominguez, 21 July 1989 (fl), Liede & Conrad 2
(UBT); Hacienda Monserrate, Purpus 9078 (NY). езш
ea: Cerro de Picardo, July 1914 (fl). Purpus 7273 (NY).

у Guay nubiles: 5

Linnaea

N

. Metastelma barbigerum Scheele.
21: 760. 1848. Cynanchum barbigerum
(Se a Shinners. Field & Lab. 19: 65. 1951.
TYPE: U.S exas: Comal Co., New Braun-
fels. jon 1846, E. Lindheimer 459 (lectotype.
designated by Blankinship (1907: 143). MO:
isotypes, GH not seen, NY!). Figures 4a-1. 5.

2a. Metastelma barbigerum var. barbigerum
Plants ascending, 30-80 cm high; shoots annual,
glabrous. Leaves with petioles 2-8 mm long. with 0
to 2 colleters at blade base; blades 10—40(—60) х
3—14(-20) mm, ovate, basally rounded, apically
acute, or rarely shortly acuminate, adaxially isolat-
edly covered mainly on veins and margins with
flexuous to recurved trichomes, 250—300 jum long,
abaxially glabrous. Inflorescences always one рег
node, 2 to 5
chronously, оня ае subsessile to sessile; floral
bracts 0.6— . 0.2 mm at the base, ovate;
pedicels 4— 6 1 mm bon glabrous. Floral buds 3-3.5
conical to elongated-

2- to 6-flowered, flowers open syn-

mm long, 1-1.5 mm diam..
conical: calyx basally fused, rotate to campanulate,
abaxially glabrous: calyx lobes 0.8-1.2 X 0.5-0.7
mm, ovate, apically acute; corolla 3.2-5.2 mm long.
glabrous,

abaxially white to cream (when dry).

adaxially white, with slightly verrucose trichomes,
200—500 um long, forming a woolly beard on the
apical parts of the lobes and downward-directed
hispid stiff trichomes, 300-500 um long. on the
central parts of the lobes; lobes fused to ca. % of
total corolla length, 0.8—1 mm wide, straight, erect,
oblong to lanceolate, apically often rather abruptly
recurved, occasionally twisted;

narrowing, acute,

gynostegial corona 1—1.3 mm long. equaling to lon-

ger than the gynostegium; lobes erect to inflexed.

attached at the base of the stipe with a distinct
hook-shaped base, laminar to solid, subulate. Gy-
nostegium 0.7—0.9 mm high, 1-1.2 mm diam., оп
a stipe 0.5-0.7 mm long: anthers about as high as
broad, trapezoidal, abaxially planar: anther wings
400 jum long. extending along the entire length of
the anther, anther wings of adjacent anthers par-
allel to each other, centrifugal: connective append-
ages 200—300 um lang: 200-300 um wide, equal-
ing the slightly inflexed:
pollinarium with мерин 400 pm long, be-
tween 1.5 times and twice as long as broad, ovoid:
caudicles 250 um long, geniculate;
pollinia apically attached to the caudicles, ca. 400
um long, 250 um wide, ovate in cross section, cla-
vate; style-head white, ca. 0.8 mm diam., 0.5 mm
high, upper part 0.25 mm high, equaling the lower
part, depressed-conical. Follicles always one per
flower, pendulous, 45-70 mm long. 5-6 mm diam.
fusiform, terete, apically strongly beaked, medium
seeds 5—6 mm long, 3.5—

slamen in widt

cylindrical,

to dark brown, glabrous;
4 mm wide, ovate, medium brown, seta and aseta
side smooth, marginally with 0.5-0.6 mm wide
wing with entire to slightly lacerate margin: coma
20—25 mm long.

Chromosome number. 2n = 22 (voucher: Liede
& Mere 2500 (MO, MSUN))

Phenology. Collected in flower from January to
October: in fruit from May to November.

Distribution. Coahuila, Nuevo
San Luis Potosí, Tamaulipas. U.S.A.:
. valley bottoms, in

Mexico: León.

Texas: lime-
stone hillsides, shale slopes
chaparral, brush or low forest; 30—2300 m.

Henrickson (1987:

Literature and illustrations.

Additional VRAC p MEXICO. Coahuila:
Cañon Loma Prieta, m al NE de Hipólito, 23 Oct.
1985 (fl), Villarreal et $ 3115 (LL): Sierra de Parras, 19

Aug. 1982 (fr), Cowan E (NY. TEX). Nuevo León:
W of Cerralto, 29 "d 7 (fl). Gregg s.n. (NY): S part
of Cerro Pedregoso, 1.5 E V of El Peñuelo, 18 June

1972 (fl), Chiang et al 7964 (LL); Chipinque. 1 July
fl), Barkley et al. 5 (TEX); Galeana, ca. 5 km E. of La
Poza toward Rio А E 18 Sep. 1933 (fl). Nesom et al.
7592 (LL); Galeana, Ranc ho Aguililla, 16 Sep. 1989 (fl.
fr). Hinton et al. 19732 (LL); ca. 120 km 5 of Laredo along
wy. 85 to Monterrey, 10 Oct. 1982, Henrickson 19303
(LL); near Monterrey, 2 June 1889 (fl, fr), Pringle 2856
G); Montemorelos, 8 Aug. 1989 (fl), Liede & Conrad
2610 (MO, UBT); 3 mi. W of i er Qu Gentry 6725
ARIZ); Cerca бе Monterrey, 29 June 19 P Fernándes
& Barkley 14485 (LL): Monte rey-Laredo ca. 49 km, Sa-
linas Victoria, eK 1994. (fl), Hinton et al 24258 (LL):
12.8 mi. S of Sabinas Eo on Hwy. 85, 2 July 1985
fl, fr), Cowan et al. 5359 (LL); tnde iit Bustamante
Canyon, 12 Aug. 1988 (A), Patterson 6519 (TEX): San
Augustine, Monterrey, 22 Apr. 1960 (fl), Smith M124 (LL).
San Luis Potosí: N of the Minas de San Rafael, 30 June

7

44 Annals of the
Missouri Botanical Garden

. d

E r, 1 MAG fi
AV КШ ee уута

T

AR 7
Da, .
MON.

с

H,
I DE 7
VEA

. Metastelma barbigerum var.
r. —d. Corolla а adaxial view. —e, e”. Corona and gynos-
tegium. —f. ооа оша —£. Style-head. ae Follic le iy Seed. a, b. : Correll & 1 19695. eg: Liede &
Conrad 2610. e': O'Neill 186: s Drawn by J. Conrad.

£z
—

liesnerianum. —i

Figure 4. Metastelma barbigerum. a-i. Metastelma bip ibs var. barbigerum. е'
“lo

abit ud пот rescence, —c.

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

M. barbigerum var. barbigerum

M. barbigerum var. liesnerianum

M. barbigerum var. veracruzense

онь ө

М. barbigerum var. barbigerum х М. pringlei
ы = — —

-115° -110° -105° -100°

Figure 5. Distribution of Metastelma barbigerum.

1972 (fl). Chiang et al. 8161D (LL); 15.7 rd. mi. E of El
Huizache jet. (at Hwy. 57) on MEX 80 to Cd. del Maiz..
24 Sep. 1978 (fl). Ж nrickson & Lee еу; is L). Tamau-
lipas: 9 mi. NW Chamal. just N of Ojo de Agua. 8
Feb. 1960 (fl). Jio 5063B (LL): Cuatro caminos, Hi-
dalgo. 5 June 1994 (fl). Hinton el al. 24186 (LL); ipm
24 Oct. 1978 (f). Calvert 117 (LL): 1 km antes de
Pes erca de la Laguna Salada, 22 Se ТД 1985 (fl). а
db 2 n 562 (TEX): S of Lomas del Real, 7 mi. N of main
Hwy. on dirt road just N of Altamira, 27 Oct. 1959 (fl).
Johnston & Graham 4525 (LL): Punta Algodones on N
end Y peninsula, 12 Sep. 1981 (fl. fr). Fryxell 3651 (NY.
LL): Tampico, 15 June 1897 (fl, fr), Pringle 6646 engin
NY): vicinity of Victoria, 1907 (fl). Palmer 360 (NY): :
т from Victoria on the road to Casas & Soto la Marina.
3 Oct. 1956 (fl). Martinez & Luyando F-2295 (LL): 5 mi.
N of Villagran on the Victoria- Linares Hwy., 12 Nov. 1959
(fr), Johnston & Graham 4674 (LL). State not. known:

w

northern Mexico, Wright 1676 (NY). U.S.A. Texas: Ban-
dera Co.. Rte. 470 betw. Tarpley 2 Unis: at Ио
Creek crossing. 16 May 1984 (fl), Ertter 5357 (NY): Bee

Co.. 2 mi. SW of Beeville. 17 July 19: EE (l. fr). Correll &
Johnston 19695 (NY): Brewster Co.. Big Bend. Oak
Springs Trail, 7 Mar. 1989 (fl). Liede & Меге 2 2500 (MO,
MSUN); Cameron Co.. dirt road 2 mi. N of Bayview clay

bank. 13 June 1967 (fl), Crutchfield 5000 (NY). 5 mi. V

of Boc a Chica, 15 Mar. 1966 a, Crute ch el 1125 (NY);

tmi. NE of Port Brownsville.

SIE

June 1967

(fl). S 2984 (NY): El 3 house
\

No. 2. along Resaca 3 la Rane ‘ho Vieje

. W of
Port Isabel. 26 June 1950 d. Webster & Wilbur 3060

(NY): Comal Co.. Old Bear Creek rd.

Bear Creek & Little Bear Creek. NW of New Braunfels.
2 fo 1983 N 15 4906 (NY): Duval Co.. S
884. Croft 62 (NY): Gillespie Co.. Balanced Rock, 4 mi.

N of Fredericks 1 on TX 965, 23 Aug. 19

78 (ID. Wyatt

1464 (GA); Bear Mountain, 18 Tni 1946 (fl), Correll &

Correll 12756 (NY); Kenedy Co.. Yturria Ranch, 6 May
‚ Rocky Bluffs,
ede d (NY); Live Oak М о.. пеаг Mathis, 28 June

7 57 (fl), Lundell 8734 (NY); Kimble €

1974 (fl. fr), McGee 134 (GA); Nueces

40,

Co..

Christi Bay, Apr. 1894 (fl). Heller 1559 (

along Corpus
NY): Corpus

Christi, 7 May 1920 (fl). Pennell 10220 (NY): Flour Bluff.
7 Jan. 1939 (fl), Tharp 248 (NY): Pecos Co..
Spring, New Braunfels, July 1851 (fl, fr). Lindheimer 992

(NY): Travis Co., Austin. Eastern Texas,
(NY): Barton Springs Creek, 23 July 1943 (fl. fr). Barkley
13360 (NY); Mt. Bonnel. nr. Austin, 24 June 1946 (fl. fr).
Albers et al. 46448 (S). County not known: s. coll. (Herb.

Berlandianum) 3198 (NY). Wright s.n.

1872, Ha li 5

(NY)

Comanche

21

46

Annals of the
Missouri Botanical Garden

2b. Metastelma barbigerum Scheele var. lies-
О. Williams) Liede & Meve,
comb. et stat. nov. Basionym: Cynanchum lies-
neriana L. O. Williams, Fieldiana, Bot. 34: 102.
1972. Metastelma pipi (L. O. Williams)
Liede, Novon 7: 42. 1997. TYPE: Costa Rica.
Guanacaste: vicinty of 48 11 mi. S of Li-
beria, 12 Dec. 1969, K. Daubenmire 406 (ho-
lotype, F neg. 056988!). Figures 4e', 5

nerianum (L.

Plants ascending, 80-200 cm high; subterranean
organs constituting a woody rootstock; shoots pe-
rennial, basally slightly woody with yellowish bark,
glabrous or sparsely covered along a single line
with recurved trichomes, 200-250 um long; inter-
nodes 2.54 cm long, to 1 mm diam. Leaves with
petioles 2-5 mm long, with 0 to 2 colleters at blade
blades 20-35 X 4-15
basally obtuse to rounded, apically acute to acu-

base; mm, ovate to elliptic,
minate, adaxially glabrous or with isolated recurved
trichomes, 200—300 um long mainly on veins and
margins, abaxially glabrous, Inflorescences always
one per node, 2- to 5-flowered, 1 to 5 flowers open
synchronously, sciadioidal, bostrychoid, sessile to
pedunculate with to 3 mm long peduncles, glabrous
or sparsely covered along a single line with re-
curved trichomes, 150-200 um long; rachis 1—2
mm long, straight; floral bracts 4—6 X 2-3 mm at
the base, deltoid to ovate, glabrous; pedicels 2—3
mm long, glabrous. Floral buds 2-2.5 mm long, 1—
1.3 mm diam., ovoid to conical; calyx basally fused,
rotate to campanulate, abaxially with a few tri-
chomes on the calyx tube (characteristic for this
0.2-0.4 mm,
apically obtuse to acute; corolla 2-3 mm long,

variety); calyx lobes 0.7-1 х ovale,
abaxially white, glabrous, adaxially white, with ver-
rucose trichomes, 100—150 um long, on the apical
and on the lateral parts of the lobes, and smooth,
downward-directed trichomes, 250-300 um long,
on the central parts of the lobes: lobes 0,8—1 mm
wide, suberect, apically acute, recurved, with
straight to slightly revolute margins: gynostegial co-
rona 1—1.2 mm long. equaling to slightly longer
than the gynostegium: lobes erect, attached near
the base of the stipe, laminar. ovate, with entire
margins. Gynostegium 0.4-0.6 mm high, 0.8-1 mm
diam., on a stipe 0.3-0.4 mm long: anthers broader
than high, trapezoidal, abaxially planar to convex:
anther wings 300—400 jum long, extending along
the entire length of the anther, anther wings of ad-
jacent anthers parallel to each other, in the same
plane as the anther to slightly centrifugal: connec-
tive appendages 300-400 um long, 200—300 um
wide, ovate to triangular, equaling the stamen in
width, slightly inflexed; pollinarium with corpus-

culum 150-200 um long, between 1.5 times and
twice as long as broad, ovoid; caudicles 60—80 jum
long, cylindrical to flattened, s-shaped, concave-
convex; pollinia apically attached to the caudicles,
150-200 um long, 80—100 um wide, clavate; style-
head white, ca. 0.5 mm diam., ca. 0.3 mm high.
upper part ca. 0.15 mm high, equaling to longer
than the lower part, flat to depressed-conical. Fol-
licles always one per flower, pendulous, 35—40 mm
long, 2 mm diam., terete, apically strongly beaked,
dark brown when dried, glabrous.

Phenology. Collected in flower from January to
August and in October; in fruit in January.
Distribution. Belize; Costa Rica: Guanacaste:
Guatemala: Péten; Mexico: Campeche, Chiapas, Ta-
basco, Yucatán; close to rivers, on disturbed slopes;
low altitudes, to 200 m.
Literature апа illustrations.

103, fig. 1A

Williams (1972:

Additional оү — BELIZE. Hectar
; ver, 6 Маг. 1935 (fl), Gentle 1508 (NY);
‚12 ka N of Belus. pa Aug. 1936 (fl), O'Neill
WIS): Mile 5 % Northern Hwy., 7 June 1974, Dwyer
12774 (NY): Vaca, 25 Apr. 1938 (fl), Dele 2517 (NY);
betw. Belmopan & 2 Ignacio, 13 Feb. 5 (fl), Liede
3242 (ОВТ). GUATEMALA. Petén: я Lagunas, El
Cedro, 4 Мау 1969 ^" fr), Contreras 8466 (NY, TEX);
Tikal Nat. 79 7050 ded de Santa Fe, 29 Jan. 1960, Contreras
532 (L " ). Campeche: 2 Oct. 1847 (fl)
wards s.r de Й = al Sureste de Conhuas dirección
Calcul. 150 m, 4 Aug. 1995 (fl), Gutiérrez 4632 (TEX).
e oo ate Palenque, 16 July й (fl), Машаа
3765 (LL ; 17 km N of Tuxtla Gutiérrez се road
to El Nees 30 Oct. 1965 Le Breedlove 14010 0(T
Tabasco: ае 8 July 1962 (Е
31376 (WIS
28/17 (WIS) Yucatan: lzamal,
UPS, WI

Y.
2
=
®
ч
a>
Cs

1895, Gaumer 539 (NY

2c. Metastelma barbigerum Scheele var. vera-
cruzense Liede & Meve, var. nov. TYPE:
Mexico. Veracruz: 48 km SE of Nautla, 30
Dec. 1972, J. Taylor & C. Taylor 12532 (ho-
lotype, NY!). Figure 5.

Haec varietas varietati liesneriano similis, sed differt

pedicellis calycibusque pubescentibus.

Plants ascending, 200 cm high; shoots perennial,
covered along a single, but occasionally a broad
line of recurved to flexuous trichomes, 300—400 jum
long. Leaves with petioles 2-7 mm long, with O to
blades 10-45 X 6-15
mm, basally obtuse to rounded, apically acuminate

2 colleters at blade base;
to acute, adaxially glabrous or with isolated re-
curved trichomes, 250-300 um long. mainly on
veins and margins; abaxially sparsely covered only
on the midrib with recurved trichomes, ca. 300 jum

Volume 91, Number 1
2004

Liede & Meve 47
Revision of Metastelma

long. Inflorescences always one per node, 2- to 7-
flowered, 2 to 7 flowers open synchronously, scia-
dioidal: peduncles 1—4 mm long. sparsely to densely
covered along a single line or over the entire sur-
face with flexuous trichomes, 150-200 um long:
floral bracts 040.8 X 0.2-0.3 mm at the base,
triangular to ovate, sparsely with trichomes on the
surface: pedicels 2-4 mm long. densely covered
over the entire surface with flexuous trichomes, ca.
200 um long. Floral buds ca. 2 mm long. ca. | mm
diam.. conical, with imbricate aestivation: calyx ba-
sally fused. rotate to campanulate, ciliate or abax-
ially with trichomes (mainly on the tube): calyx
lobes 1—1.2 X 0.5-0.6 mm, ovate, apically acute:
corolla rotate to campanulate, 2-3 mm long. abax-
ially white, glabrous, adaxially white, adaxially with
verrucose trichomes, 100—150 um long. on the api-
cal and on the lateral parts of the lobes and down-
250-300 um
long. on the central parts of the lobes: lobes fused

ward-directed smooth trichomes,
to ca. % of total corolla length, 0.6-0.8 mm wide.
erect to patent, ovate, apically acute: gynostegial
corona 0.8—1 mm long, equaling to longer than the
eynostegium: lobes erect, attached along the stipe.
laminar, very narrowly ovate. Gynostegium ca. 0.6
mm high, са. | mm diam., on a stipe 0.3-0.5 mm
long: anthers broader than high, trapezoidal, abax-
ially planar: anther wings 300 um long. extending
along the entire length of the anther, anther wings
of adjacent anthers parallel to each other. in the
same plane as the anther: connective appendages
300—350 um long, 250-300 um wide, ovate, nar-
rower than the stamen, slightly inflexed; pollinar-
ium with corpusculum 150-200 jum long. between
1.5 times and twice as long as broad, elliptic; cau-
dicles 50-60 um long. flattened, s-shaped, con-
cave-convex; pollinia subapically attached to the
i 200 um long, ca.

caudicles, ca. 100 pm wide,

ovoid: style-head white. ca. 0.7 mm diam ca. 0.5
mm high. upper part ca. 0.25 mm high. equaling
the lower part. flat to depressed-conical. Follicles
always one per flower. 30-40 mm long. 4-6 mm
diam., obclavate, straight, apically strongly beaked,
green-brown, glabrous: seeds 5-6 mm long. 2.5—3
mm wide, ovate, medium to dark brown, seta side
tuberculate, papillose with regularly arranged pa-
pillae, aseta side vaguely tuberculate, marginally
with 0.2-0.3 mm wide wing with denticulate mar-
gin; coma 25—30 mm long.

Phenology. | Collected in flower from August to
December: in fruit in December.

Distribution. Mexico: Tabasco. Veracruz: sand
dunes and savanna borders; 0—50 m.

Cowan & Magafia 3270 (NY) from Huimanguil-

lo. Tabasco. is not entirely. glabrous like variety
liesnerianum, but not as densely indumented as the
other Metastelma barbigerum var. veracruzense
specimens.

There is a second NY specimen of Purpus 2094.
which is referred to M. schlechtendalit var. schle-
chtendalit.

The Metastelma barbigerum complex is charac-
terized by mostly glabrous stems (but with a single
line of trichomes in var. veracuzense), conically
shaped gynostegia with obliquely protruding anther
wings (guide rails) and corona lobes that hardly ex-
ceed the anthers (Figs. la. c. e. f: compare also
1987).

fer in the attachment of the corona lobes, which is

Henrickson, The two southern varieties dif-
not as distinctly hook-shaped as in the typical va-
riety. The distribution of this complex is confined
to the eastern landmasses surrounding the Gulf of

Mexico.

Tabasco: Huimanguillo, km
39.7 de la desviación de Humanguillo hacia Fco.
10 Oct. 1980 (f). Cowan & Magaña 3270 (NY). Vera-
eruz: hte. 180, 130 IW Catamaca. 16 Sep. 1970 (fl).
Burch 2984 (NY): rw pid s de la planta Laguna Verde.
11 vw. 1975 (fl), Dorantes 5270 (NY): about 4.5 mi. W
of Palmilla along pui through Huatusco, 10 Aug. 1971
(fl). Stevens 1409 ( : Tecolutla. 20 Dee. 1963 (fl. fr).
Cavender s.n. (WIS): zi uapan and vicinity, Nov. 1906 (fl).
Purpus 2094 (HBG, NY).

Paratypes. MEXICO

Rueda,

3. Metastelma californicum Benth.. in Hinds.
R. B., Bot. Voy. Sulphur: 33, pl. 18. 1844. Cy-
nanchum californicum (Benth.) Moran, in Lev-
in & Moran, Vascular Fl. Isla Socorro Mexico
(Mem. San Diego Soc. Nat. Hist. 16): 26. 1989.
TYPE: Mexico. Baja California: Magdalena
Bay, С. Bentham s.n. (holotype. K!).
6a-f.

Figures

За. Metastelma californicum Benth. subsp. eal-
ifornicum

Plants ascending, 50-150 em high: shoots an-
nual, basally woody, with gray-brown bark, glabrous
or isolatedly glabrescent along a single line with
flexuous trichomes, 200—300 um long: internodes
2—4 cm long, 0.5-0.8 mm diam. Leaves with peti-
oles 3-6 mm long. with 2 colleters at blade base:
blades 10-20(-25) х 4—10(-14) mm. ovate to el-
liptic, basally rounded, apically acute to acuminate.
adaxially sparsely covered on the midrib and the
200—300 um

long, abaxially glabrous. Inflorescences always one
8 ys l ›

margins with flexuous trichomes,

per node, 2- to 6-flowered, 2 to 3 flowers open syn-
chronously, sciadioidal, floral bracts
0.5—0.6 X 0.2-0.3 mm at the base, triangular, gla-

subsessile:

48

Annals of the
Missouri Botanical Garden

„Kéi
Amie 409
as Wi WS
E ASA

Wr \
. .

7 y me
{, И М, E Ng
A

-
\ i
1 mm
Figure 6. усун Ima californicum subsp. californicum.
lobe, adaxial view. —d. Gynostegium and corona. —e

Conrad 2955. us by J. Conrac

brous; pedicels 3—4 mm long, glabrous or with a few
isolated trichomes. Floral buds ca. 2 mm long. ca.
1.5 mm diam., ovoid; calyx basally fused, campan-
agn vu glandular, glabrous: calyx lobes 1—

).4—0.6 mm, ovate, apically acute; corolla
pan Из to rotate, 2.5—3.5 mm long, abaxially
glabrous,

200-250

white, purplish along the main nerves.
adaxially white, with verrucose trichomes,

um long. on the apical and on the lateral parts of

the lobes and with smooth, downward-directed tri-

chomes, 180-220 jum long, on the central parts of

. Shoot и inflorescences. —b. Flower. —c. Corolla
Style-head. a: Brandegee s.n. b-f: Liede &

Pollinarium.

the lobes: lobes basally fused, 1-1.2 mm wide, pat-
ent to erect, ovate, apically acute to obtuse; gynos-
tegial corona 1.3-1.5 mm long, slightly longer than
the gynostegium; lobes erect, attached directly un-
lanceolate. Gynos-

derneath the anthers, laminar,

tegium ca. | mm high, ca. 0.9 mm diam., sessile:
anthers higher than broad, rectangular, abaxially
gibbous; anther wings ca. 500 рт long, extending
along the entire length of the anther or beyond,
anther wings of adjacent anthers divergent toward

the base, in the same plane as the anther; connec-

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

tive appendages 300-400 um long. ca. 300 рт
wide, ovate, equaling the stamen in width. slightly
inflexed: pollinarium with corpusculum. 140—150
um long. between 1.5 times and twice as long as
broad, ovoid: caudicles 60-70 рт long, cylindrical
to flattened, straight. ascending, slightly thickened
at the insertion of the pollinium: pollinia subapi-
cally attached to the caudicles, 180-220 jum long.
80-90 um wide, ovate in cross section, ovoid: style-
head white. ca. 0.5 mm diam., ca. 0.4 mm high,
upper part ca. 0.2 mm high. equaling the lower

vart, conical. Follicles always one per flower, 50—
60 mm long, 4-6 mm diam., fusiform, terete. api-

cally strongly beaked. wingless, dark brown. gla-
brous; seeds 5-6.5 mm long. 2.5-3 mm wide, ovate,
dark brown, seta and aseta side tuberculate, mar-
ginally wingless, entire: coma 10-20 mm long.

Phenology. Collected in flower from October to
April and in July and August: in fruit in December,
February, March. and October.

Distribution. Mexico: Baja California, Sinaloa,
Sonora, Revillagigedo Islands: on rocky slopes and

in sandy washes, very dry desert. vegetation; 0—
6 m.

Literature and illustrations. Bentham (1844: pl.
18).

Additional specimens | examined. MEXICO. Baja Cal-
ifornia: 3.2 mi. NW of Arroyo Palmarito via Hwy. 1. 21
July 1990 (fl. fn. — & Van Devender 7661 (ARIZ):

E co. 21 Mar. ү (fl. fr). Shreve 7197

» of Arroyo Sec

(ARIZ): Catavina, 76 mi. El Rosario on Mex. Hwy.
1, 13 Dec. 1977, Nixon & n 831 (LL); 2 mi. NW of
Catavina, 29 Apr. 1980 (fl). Davis & ADR 66297
(В); Cerro Tordillo & vicinity, Systema de la Sierra Vis-
caino, 12 Mar. 1947 (Н), Gentry 7438 (ARIZ): Escondito
Creek, 7 Mar. 1934 (fl. fr), Shreve pons (ARIZ): Escon-
dido Canvon betw. Punta Prieta M ocean, 7 Mar. 193 | (fl)
Ferris 8589 (NY): 8 mi. N of Mt. Mesquital Grande, 9
Feb. 1935 (fl), Haynes & Stewart s.n. (NY); O mi. S of
Laguna Chapala к а. 17 Oct. 1959 (f, Wiggins 15048
(ARIZ); Picacho de Santa Clara, Nov. 1947 (fl), Gentry
7716 (ARIZ): Playa S бай Pedrito. Los Cerritos, al SW de
Todos Santos, 13 Oct. 1985 (fl. fr). Tenorio et al. 10441
(MO); 10-20 km N of Puerto Santa Catarina on rd. to
Rancho Santa Catarina, ] ir 1985 (fD. Breedlove 62261
(NY); 20-30 mi. 5 of Punta Canoas along da to Punta
Cono, 27 Feb. 1986 (fl). ا‎ 62528 (LL); 12.1 mi.
(by rd.) N of Pi i 3 we 17 Oct. 1967 (fl). x wd &
Turner 67-64 (ARIZ): 2.5 mi. 5 of 9 9 Prieta, 17

Oct. 1959 (fl. A Wiggins 15085 (ARIZ); just 5 of Rosar-

ito, ^ Mar. 1979 (fl. fr). 5 & Bowers 2119
(ARIZ); Todos Santos, ca. 8 km on track to Sierra 1 aguna,
20 ppa 1992 (fl. fr). Liede & Conrad 2955 (l LM): Todos

sete ys S.H. S ae Inlet.
Magdalena Bay. 10 Aug. (fl), Howell 10639 (NY).
Sinaloa: Isla Tac hec hilte. : en m. 20 Jan. 1945. Gentry
7136 (ARIZ NY). E sla San уе Nolasco, E
side of ad, Nov. . Felger 9635 ане 5 Li
Las los ‘as on the coast = de Gulf of California. ‘eb.

1992 (fl. fr), Van Devender et al. 92-121 (ARIZ): ps

Santos, Jan. 1890 (fl).

1995,

C homajabire s, 1.8 mi. N of Huatabampito, 23 Dec.
Revil-

Fishbein & Mc Mahon 2750 (ARIZ), 2769 (ARIZ).
lagigedo Islands: Socorro Island. 24 May 1903, Barkelew
217 (ARIZ, NY).

3b. Metastelma californicum Benth. subsp.
lanceolatum (Schltr.) Liede & Meve. comb.
Basionym: Metastelma lanceola-
Bull. Herb. Boissier 6: 840. 1900.

San José Pass.

et stat.
tum Schltr.,
TYPE: Mexico. San Luis Potosí: $
12 July 1890, C. G. Pringle 3138 A
M!: HBG!, NY!

nov.

designated here, isotypes,

Figures 7a-g. 8.
Ditassa mexicana Brandegee. Calif. Publ. Bot. 10:
414. 1924. Syn. nov. T
cienda Montserrate, Sep. 1923, (

(holotype, UC 220412 not seen: не GH! NY!)

Univ.
"PE

Plants ascending. to 250 cm high: shoots peren-
nial. basally woody, with brownish bark. sparsely
covered along a single line with recurved tri-
chomes, 150—300 рт long: internodes 1.7 cm
long. to 1 mm diam. Leaves with petioles 3—5 mm
long. with 2 colleters at blade base: blades 15-35
X 3-16 mm, ovate to oblong, basally rounded, api-
cally acute to acuminate, adaxially sparsely cov-
ered only on the midrib and the margins or over
the entire surface (Roe & Roe 1885) with erect to
recurved trichomes, 200—350 рт long. abaxially
glabrous (occasionally with a few trichomes on the
midrib). Inflorescences always one per node, 4- to
7-flowered, 1 to 7 flowers open synchronously, scia-
dioidal, subsessile; floral bracts 0.5-0.6 X 0.3-04
mm at the base, triangular, glabrous or ciliate: ped-
icels 2-3 mm long. glabrous or sparsely covered

along a single line with flexuous trichomes. ca. 200
um long (Roe & Roe 1885). Floral buds 2-2.5 mm

1.3-1.5 mm diam., ovoid: calyx basally fused,
campanulate, abaxially glabrous or with trichomes
on the tube (Roe & Roe 1885): calyx lobes 0.8—1
X 0.4-0.6 mm, ovate, apically acute; corolla rotate

long,

to eyathiform, 2.5—3 mm long. abaxially greenish
adaxially white or cream, with verrucose tri-
chomes, 120-180 um long, on the apical and on
the lateral parts of the lobes and smooth trichomes.
180—200 um long, on the central parts of the lobes:
1—1.2 mm wide, patent. ovate.

white,

lobes basally fused,
apically acute to obtuse: gynostegial corona 0.6—
1.2 mm long. equaling to longer than the gynoste-
gium; lobes erect, attached directly underneath the
anthers, laminar, ovate, apically acute to longly
acuminate. Gynostegium 1-1.3 mm high. 1.2-1.5

mm diam., sessile: anthers about as high as broad.
anther wings 500—

rectangular, abaxially gibbous:

600 um long. extending along the entire length of
the

anther, anther wings of adjacent anthers par-

Annals of the
Missouri Botanical Garden

ж

ä

(Lua LET!

S He
К * =

V bay ^
Ve

үз,
NS
NX
NE E

"EC

EN

We

m t Ам N

М,

mE

Figure 7. Metastelma californic um шк lanceolatum. —а. Habit. —b. Shoot with inflorescence. —c, c'. Flower.
— d. ( ‘orolla lobe, adaxia view. —e, e' na and gynostegium. —f. Pollinarium. —g. S
drawn by J. Conrad. e”, e”. Roe & Roe 1885. executed by U.

x. Style-head. a-g: Purpus 9167,
Meve after sketch by J. Conrad

Volume 91, Number 1

Liede & Meve
Revision of Metastelma

2004
ГЕЯ
М. wi T , $
ed س‎ | |p|]
AA | | 2); |
A | $
E Lem 88. — ve | — 7 NM 35?
f À | | | | | اہ‎ ~ A, 14 |
. | :
V і i
os: | | | X — M
\ | | |S „Л daa o
o. i == Х - X crap ГТ" 30
" * 1 iz * N уу
| ea S "uii
s 4 . n Б | | A |
p e.
4 t X. y ‘
| Б 4\
etj AS
le | a A ‚ J |
- AAA AAA : 25°
e ^ ]
| ү у ү 44 i |
] PY y | Te \
Е =y Ж 4 — 4 1 ыч i= 2 > 4 20°
| hs de ROS | А
| e | i > А + ; = к< 07
| | "nM "a 4 4 44 s — |
N californicum ssp. californicum : | Т F |
| | А M.californicum ssp. lanceolatum 4 i |
|
-120° -115° -110° -105° -100° -95° -90°

Figure 8. Distribution of Metastelma californicum.

allel to each other, in the same plane as the anther:
1. 400

connective appendages ca. 400 um long. cz
width,

pm wide, ovate, equaling the stamen in
slightly inflexed: pollinarium with corpusculum
160-180 um long. between 1.5 times and twice as
long as broad, ovoid; caudicles 60-80 um long.
cylindrical to flattened,
convexly recurved; pollinia subapically attached to
the caudicles, 280-300 um long, са. 120 рт wide,
ovate in cross section, ovoid: style-head white, 0.7—
0.4—0.6 mm high. upper part 0.3—
longer than the lower

+ horizontal to

straight,

0.9 mm diam..
0.4 mm high. equaling
part. conical. Follicles always one per flower, 35—
45 mm long. 4-6 mm diam., obclavate. terete, api-
cally strongly beaked, dark brown. longitudinally
grooved: seeds ca. 5 mm long. ca. 3 mm wide. ovate,
medium brown. seta and aseta side smooth, mar-
ginally with 2 mm wide wing with denticulate mar-
gin: coma 15-25 mm long.

Phenology. Collected in flower in February.

May. and from July to October: in fruit in February,

August, and September.

Distribution. Mexico: Chiapas, Guerrero, Hi-
dalgo. Jalisco. México Distrito Féderal, Morelos.

Oaxaca, Puebla, San Luis Potosí. Yucatán: on lime-
stone slopes in scrub vegetation and deciduous
tropical forest: 1000-2200 m.
For Metastelma lanceolatum.
cited the type as follows:
pes prope Zoquitlan, flor. Jun. C. Seler & H.
Seler ° However. the first set of collections of
Seler n бе was housed in B (Vegter, 1986), and
the type of M. lanceolatum was probably destroyed
during the second World War. It is not duplicated
in any of the herbaria consulted for this study. The
specimen selected as neotype (Pringle 5136. NY)
“Metastelma lanceolatum

Schlechter (1906)

“Mexico. Oaxaca: Distr.

bears the annotation
Schltr.” in Schlechters own handwriting.

The protologue of Ditassa mexicana states. ex-
plicitly “corona duplici." which is the generic char-
acter of Ditassa. No other "Ditassa^ specimen ex-
cept for the type of Ditassa mexicana was ever
collected in Central America. However. none of the
flowers examined had a double corona. This spec-
imen exhibits the characters of Metastelma califor-
nicum subsp. lanceolatum. so that Ditassa remains
a genus restricted to South America.

Metastelma californicum is easily distinguished

Annals of the
Missouri Botanical Garden

from all other Central American Metastelma species
by a stout, sessile gynostegium with anther wings
(guide rails) as long as the gynostegium. The corona
is spreading and hardly exceeds the gynostegium.
Morphological differences between the two subspe-
cies of M. californicum mainly concern the shape
of the corona lobes. As separation is both geograph-
ical and ecological, with the typical subspecies oc-
curring in very dry desert vegetation below 640 m,
and M. californicum subsp. lanceolatum in scrub
vegetation and deciduous tropical forest between
1000 and 2200 m, subspecific rank, as in the par-
allel case of M. arizonicum, is warranted.

— онн 5 ME XICO. sei
Federal: n Hwy
l i "Roe 1885 (NY. WIS); Volcán,
2 Feb. 1935 (fl, fr), Hinton et al. 7310 (NY). Guerrero:
10 m Copac Cp 5 Aug. 1970 (fl), Boege 1438
R); La Posa del Lago Tres dd чорва abana, 19 Sep.
pus (fl). Boege à (FR) I lidal donde 'a de Tolan-
tongo, 8 Aug. 1991 (fl). id „ МҮ); slopes
of Barranca de шл 8 Aug. 1948, n & Wood 4409
(LL); El Capulin, near km 1 ^ on highway be
& пага 4 Aug. 1948
(LL); Jacala, 2 July 1939 Ny Chase 7418 (ARIZ, NY).

L). Me
9 (fl), Pringle 10838 (ARIZ, TEX). Oa-
idein Galeotti 1571 (NY). Puebla: 11 km al
SE de San Juan Ixc ке 5 du 1986 (fl), Salinas &
Tenorio 3294 (ARIZ, LL). San Luis Potosí:

Pedro, 29 July 1934 (fl). edm 17729 (NY);
. 1939 (fl, fr), Shreve 9312 (ARIZ); Hwy. Valles to
25 May 1981 (fl), Fry xell & An-
de 7 (NY). Yucatán: above Calcehtok, 21 Feb.
1982 (fl), White & Mott 74 (NY).

4. Metastelma cuneatum Brandegee, Zoe 5:
216. 1905. TYPE: Mexico. Sinaloa: Yerba
Buena, vicinity of Culiacan, 10 Sep. 1904, T.
S. Brandegee s.n. (holotype, UC not seen; iso-
types, GH!, US). Figures 9a—h,

Plants ascending, 200—300 cm high; shoots pe-
rennial, basally woody with grayish brown bark,
sparsely to densely covered along a single line with
erect to recurved trichomes, 300—400 рт long; in-
ternodes 1.8-3 cm long, ca. 1 mm diam. Leaves
with petioles 2—4 mm long, with 2 colleters at blade
base; blades 15-20 х

basally obtuse, apically obtuse or acuminate, adax-

3-7 mm, ovate to oblong,

ially sparsely covered, only on the midrib with ap-
pressed to recurved trichomes, 200-300 um long,
abaxially glabrous. Inflorescences one, occasionally
two per node, 3- to 8-flowered, 2 to 6 flowers open
synchronously, sciadioidal; peduncles 0.5-3 mm
long, sparsely covered along a single line with erect
trichomes, 150-200 um long; floral bracts 0.2—0.5

).2-0.3 mm at the base, triangular, elongated-

triangular or ovate, with scattered trichomes on the
surface; pedicels 3-4 mm long, glabrous, isolatedly
to sparsely covered along a single line with flexuous
trichomes, 200-250 um long. Floral buds 1-1.3
mm long, 0.8-1 mm diam.;
of its length, campanulate, abaxially glandular; ca-
lyx lobes 0.6-0.8 X
acute; corolla rotate, 1.5-2 mm long, abaxially yel-
lowish green, glabrous, adaxially white, with ver-

calyx fused for ca. Y

.2-0.3 mm, ovate, apically

rucose trichomes, 50-100 рт long, on the apical
and on the lateral parts of the lobes; and with a few
slightly longer, retrorse and smooth trichomes on
the central parts of the lobes; lobes basally fused,
0.3-0.5 mm wide, erect to incurved, ovate, apically
acute; gynostegial corona 0.5—0.7 mm long, equal-
ing to shorter than the gynostegium: lobes erect to
inflexed, attached directly underneath the anthers,
laminar, ovate to triangular. Gynostegium 0.5-0.6
mm high, 0.7—0.8 mm diam., sessile to on a column
ca. 0.3 mm long: anthers about as high as broad,
rectangular, abaxially convex; anther wings

500 um long, extending along the entire length of
the anther, anther wings of adjacent anthers par-
allel to each other, basally widened, in the same
plane as the anther, basally forming a distinct
"mouth" with the basal lateral margin of the anther;
connective appendages ca. 500 jum long, ca. 400
pm wide, ovate, equaling the stamen in width,
strongly inflexed; pollinarium with corpusculum ca.
120 um long, more than twice as long as broad,
slenderly oblongoid; caudicles ca. 100 um long,
cylindrical, s-shaped, convex-concave, thickened at
the insertion of the pollinium; pollinia subapically
attached to the caudicles, ca. 150 um long, ca. 50
um wide, ovate in cross section, reniform; style-
head ca. 0.7 mm diam., 0.35 mm high, forming
distinct noses at upper ends of corpusculi, upper
part ca. 0.15 mm high, shorter than the lower part,
depressed-conical. Follicles always one per flower,
60—80 mm long, 4—5 mm diam.,
siform,

very slender fu-

terete, apically shortly beaked, grayish

brown, glabrous; seeds 6-7 mm long, 3-3.5 mm
wide, pyriform, medium brown, seta side vaguely
tuberculate, aseta side smooth, marginally with
0.2-0.3 mm wide wing with denticulate margin;
coma 25—30 mm long.

Phenology. Collected in flower in September
and from November to January; in fruit in January.

Distribution. Mexico:
and Sinaloan thornscrub; 0-25 m

The inconspicuous indumentum of the corolla,

Sinaloa, Sonora; coastal

the anther wings forming a distinct “mouth,” and

the very slenderly oblongoid corpusculi carrying

Volume 91, Number 1 Liede & Meve 53
4 Revision of Metastelma

с. Flower. —d. Corolla lobe. adaxial

Figure O. Metastelma cuneatum. а. Shoot with follicle. —b'. Inflorescence.

o
view. —e. Gynostegium and corona. —f. Pollinarium. —g. Style-head. —h”. Seed. a. eg: Friedman 150-95. b: van
Devender et al. 1284. h": Friedman 199-95. Executed by U. Meve after sketch by J. Conrad.

Annals of the
Missouri Botanical Garden

O Metastelma cuneatum
А Metastelma latifolium |

Ф Metastelma minutiflorum

30°

— -> A
A

25°

-115° -110°

Figure 10.

markedly s-shaped caudicles make this coastal res-
ident an easily recognizable species.

Additional specimens examined.
in arroyo d оа, 1.5 K

MEXIC Sinaloa:
m NE of Cana, 15 m,
17 Jan. 19¢ 5 (fl), Frie Ed 015-95 (ARIZ); е
Muerto, 1.5 Т. NNW of Ca ›аһштоа on rd. to С Bo
17 Jan. 1995 (fl), Feldman. 104-95 (ARIZ); 9.8 km W
and 5 km N of Mex 15 on Las Bon 'as Rd., 20 Jan. 1995
fr), Friedman 150-95 (ARIZ): 6.25 km E of Camahui-
roa on rd. to Diez de Abril, 20 Jan. 1995 dl, fr), Friedman
199-95 (ARIZ): 4.4 km SW Ejido Tierra y Libertad. 1 km
Von dirt rd., 19 Sep. 1994 a. Friedman rines 94 (ARIZ).
Sonora: along rd. to Bachoco, ca. 3.5 mi.
24 Dec. 1995 (fl), Fishbein 27. 59 (ARIZ
the coast of the Gulf of California, 1 Feb. 1992 (fl, fr),
Van Devender et al. 92-133 (ARIZ); 1.5 km NNW of Ca-
mahuiroa on rd. to Las Bocas, 23 Nov. 1993 (fl. fr). Van
Devender 93-1253A (ARIZ); 2 km W of Tierra y Libertad
on northern rd. to nU ya, 24 Nov. 1993 (fl), 150
Devender et al. 93-1284 (ARIZ); mouth of arroyo Masiacz
Las Bocas on the Gulf of California, 22 Sep. 1994 (fl), Van
Devender & Yetman 94-698 (ARIZ).

—

E of Las Bocas,
); Las Bocas on

20°
-105° -100°

Distribution of Metastelma cuneatum. M. latifolium, and М. minutiflorum.

э. Metastelma eliasianum Dugand, Caldasia 9:
445. 1966. TYPE: Colombia. Bolivar: N of Ar-
jona, 30-50 m, 15 Nov. 1926, E. P. Killip
А. C. Smith 14531 (holotype, US 1.350.518
not seen; isotypes, GH not seen, NY!, P!). Fig-
ures lla-f, 12

C ynanchum infimicola L. O. Williams, Ann. Missouri Bot.

"ard. 55: 48. 1968. Syn. nov. Metastelma о

(L. О. о W. D. Stevens, 5
1988. TYPE: = "s ere K-2 го;

1967, J. D. r & S. | Hayden 7. 7540 Гата

type, F!; pl MO not abe

: 00).

Plants ascending: shoots perennial, basally
woody, with yellowish to brownish bark, sparsely
covered along a single line with recurved tri-
chomes, 150-250 um long; internodes 3-7 cm
ong, 1-1.5 mm diam. Leaves with petioles 6—10
mm long, with 2 or 3 colleters at blade base; blades
25—50 X 8—30 mm, ovate, basally rounded to cu-

Volume 91, Number 1

Liede & Meve 55

Revision of Metastelma

ois! 7 go
£x Е
\

TE

\

Figure 11.
d. Gynostegium and corona.
Drawn by J. Conrad.

. Pollinarium. H.

neale, apically very acute, adaxially isolatedly cov-
ered only on the midrib with appressed trichomes,
ca. 250 um long, abaxially glabrous. Inflorescences
always one per node, 4- to 7-flowered, 2 to 4 flowers
open synchronously, bostrychoid; peduncles 5-15
mm long, sparsely to densely covered along a single
line with recurved trichomes, 200-250 рт long;
rachis 0-5 mm long, angular; floral bracts 4—5 X
3—4 mm at the base, ovate, papillose: pedicels 2-5

Metastelma para —a. Shoot des inflorescences. —b. F
Style-head. a: Ие

KES
ES

—

>
3
3

A
AER:

e

"PI

Corolla lobe, adaxial view. —

Allen & Seibert 1499. bf: Duke 12414.

"lower. —¢

mm long, glabrous. Floral buds ca. 1.5 mm long.

ca. 1 mm diam., cylindrical; calyx basally fused,
cyathiform, abaxially glabrous or with a few sparse
trichomes on the tube; calyx lobes 0.8-1 х 0.4—
0.5 mm, ovate, apically acute; corolla campanulate,
2-2.5

adaxially white, with verrucose, 120-150 um long
trichomes on the apical parts of the lobes: lobes
fused for ca. % of total corolla length, ca. 1.5 mm

mm long, abaxially greenish white. glabrous.

Annals of the
Missouri Botanical Garden

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e Metastelma eliasianum ^m E — ^
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А Metastelma pedunculare * „% T
XA N
ш Metastelma stenomeres QA) 1
3
ү
2
— ae |
| ل‎ — - 5°
-100° -95° -90° -85° -80° -75°
Figure 12. Distribution of Metastelma eliasianum, M. pedunculare, and M. stenomeres.
wide, patent, oblong, apically acute; gynostegial co- Phenology. Collected in flower in May and

rona 1-1.2 mm long, equaling the gynostegium;
lobes erect, apically reflexed, attached at the base
of the stipe, laminar, oblong. Gynostegium ca. 0.3
mm high, ca. 0.8 mm diam., on a stipe 0.8-1 mm
long; anthers broader than high, rectangular, abax-
ially planar; anther wings 300 um long, extending
along the entire length of the anther, anther wings
of adjacent anthers parallel to each other, in the
same plane as the anther; connective appendages
ca. 150 um long, ca. 300 um wide, ovate, equaling
the stamen in width, strongly inflexed; pollinarium
with corpusculum 100 um long, about twice as long
as broad, margins of the corpuscular cleft parallel:
caudicles 60-80 jum long, cylindrical, s-shaped,
convex-concave; pollinia apically attached to the
caudicles, ca. 350 jum long. ca. 70 jum wide, ovate
in cross section, clavate; style-head white, ca. 0.7
mm diam., ca. 0.2 mm high, flat. Follicles one per
flower, 50—60 mm long, 3—4 mm diam..

obclavate tc

narrowly

fusiform, terete, apically strongly

=

beaked, wingless, medium brown, glabrous; seeds
unknown.

from July to September.

Distribution. Colombia. Panama: Coclé, Canal
Zone, Panamá; savanna and thickets; 0-200 m. one
2, NY) from 700 m.

Metastelma E is most closely related to

record (Tyson et al. 3962

M. pedunculare and shares with it the long stipe,
the tiny, ca. 0.3 mm high gynostegium, and a sim-
ilar pollinarium structure. However, the long corona
lobes of M. eliasianum originate at the base of the
stipe, while the shorter corona lobes of M. pedun-
culare originate just underneath the gynostegium.
Metastelma eliasianum thus takes an intermediate
position both in corona morphology and geograph-
ical distribution between the truly Central Ameri-
can M. pedunculare and the South American M.
parviflorum, in which the attachment of the corona
lobes has moved even further away from the gy-
nostegium and onto the base of the corolla.

Based on specimen records, Metastelma eliasian-
um might be more widely distributed in South
America, but this is beyond the scope of the present
revision.

Volume 91, Number 1
2004

Liede & Meve 57
Revision of Metastelma

б PANAMA. Coclé
betw. Las Margeritas & El Va d 1938 (fl), Won.
65 (NY). Panamá: E mi. S of El Valle

May 1966 (fl), Tyson et al. 3962 (NY); nr. Rio Mar, Е
July 1967 (Н), Duke 12414 (NY. WIS): Taboga Island.
Sep. 1962 (fl), Dwyer 2809 (NY), 20 May 1911 (fl), а
3539 (NY), 23 July 1938 (fl). Woodson et al. 1499 (NY).

Additional specimens

T

6. Metastelma latifolium Rose, Contr. U.S. Natl.
Herb. 1: 106. 1891. TYPE: Mexico. Sonora:
Alamos, 16 Sep. 1890, E. Palmer 665 (holo-
type. US not seen: isotypes. GH-2 not seen.
NY). Figures 10. 13a-f.

Plants
woody, with blackish brown bark, sparsely covered

ascending; shoots perennial, basally
along a single line with flexuous trichomes, 350—
450 um long; internodes 2.5-6 cm long, | mm
i with 2

diam. Leaves with petioles 3-5 mm long,

colleters at blade base: blades 25-55 X 7-15 mm.
ovate, basally obtuse, apically acute to acuminate.
adaxially sparsely covered only on veins and mar-
300—400 um long,
covered, only on the midrib
300—400 um long. /nflo-

rescences always one per node, 2- to 12-flowered, 2

gins with flexuous trichomes,
abaxially isolatedly
with flexuous trichomes,

to 6 flowers open synchronously, sciadioidal (some-
times a little elongated); peduncles 1—4 mm long.
densely covered along a single line with flexuous
trichomes, 300—400 um long: floral bracts 0.5—0.7
0.2-0.3 mm at the base, ovate to triangular, gla-
brous; pedicels 2-5 mm long, glabrous. Floral buds
1.6-1.8 mm long. 0.8-1.1 mm diam., ovoid; calyx
basally fused, campanulate, abaxially glabrous; ca-
lyx lobes 0.8-0.9 x 0.4-0.5
acute; corolla campanulate, 1.7-2 mm long, abax-

mm, ovate, apically

ially white, glabrous, adaxially white, with verru-

cose trichomes 100—120 um long on the apical and
on the lateral parts of the lobes, and with down-
ward-directed smooth trichomes 150-200 рт long
on the central parts of the lobes: lobes basally
fused, 0.4—0.6 mm wide,

cally acute; gynostegial corona 0.5-0.6 mm long,

erect to patent, ovate, api-

shorter than to equaling the gynostegium; lobes
erect, laminar, oblong. Gynostegium 0.1-0.9 mm
high. 0.9-1 mm diam.. subsessile; anthers about as
high as broad, rectangular, abaxially planar: anther
wings 350—400 um long, extending along the entire
length of the anther, anther wings of adjacent an-
thers parallel to each other: connective appendages
са. 250 jum long, ca. 350 wm wide, ovate, equaling
the stamen in width, slightly to strongly inflexed:
pollinarium with corpusculum ca. 120 jun long, be-
tween 1.5 times and twice as long as broad, ovoid:
caudicles 50-60 um long, cylindrical, geniculate,
thickened at the insertion of the pollinium: pollinia
subapically attached to the caudicles, ca. 140 jum

long, 50-60 um wide, ovate in cross section, ob-
0.3—0.4 mm
high, upper part 0-0.2 mm high, shorter than to

longoid; style-head ca. 0.7 mm diam.,
equaling the lower part, flat to umbonate. Follicles
and seeds unknown.

Phenology. Collected in flower in March and
April and from August to October.

Distribution. Mexico: Chihuahua, Sonora; open
places in mixed deciduous hardwood forests and
tropical deciduous forests; 250-1200 m.

Literature and illustrations. Wiggins (1940: 82,
pl. 18).

Metastelma latifolium and М. minutifolium con-

stitute a pair of closely related, very small-flowered

a

corolla less than 2 mm long) species with different
ecological preferences. Metastelma latifolium. char-
acterized by ovate, apiculate leaves, shoots with
one line of trichomes, pedunculate inflorescences,
ovoid to oblongoid pollinia and flat to umbonate
style-heads, is an inland and upland species, while
M. minutiflorum, characterized by linear to slen-
derly lanceolate leaves, shoots with two lines of tri-
chomes, subsessile inflorescences, reniform pollin-
ia, and conical style-heads, prefers habitats close
to the coast. A detailed analyis of the tiny pollinaria
and the style-heads is necessary for secure deter-
mination (cf. Fig. 13).

Additional м examined. MEXICO. Chihua-
hua: Guasaremos, Rio Mayo, 10 Aug. 1936 (fl), Gentry
2373 (ARIZ). Sonora ca. 40 mi. NE й
1980 (fl). Lehto 24882 (ARIZ): Cer-
ros Colorados: 34 a E of El Tabelo on rd.
Verdes, 29 Oct. ‚ Van Devender et al. 95-118
(ARIZ); E Tesopaco, along new rd., р
Аир. 1976 8, о 76-322 (ARIZ); Sierra de Ala-
of Alamos, 31 Aug. 1996 (tl). Steinmann
PU Sierra d Alamos, Arroyo Agua
Escondida, 20 Aug. 1994 (fI), Fishbein et al. 1903 (ARIZ):
Sierra de Alamos, Canon Chapotes 19 Mcr 1994 (fl), Fish-

bein et al. 1606 ARIZ); along Hwy. 16, 3.5 mi. of
epoca, 11 mi. E uf Puerto de la Sam 6 Sep. 1995 (fl).
ИА 2460 (ARIZ): Rancho las Uvalamas, 25 Aug.

0 (fl), Martin & McWorther s.n. (NY); 26.9 km SE of
is Yaqui on MEX 16 (Rancho 3 Mula), 21 Sep. 1997
(fl), Reina et al. 97-1087 (ARIZ, LL).

7. Metastelma das RE: O. Williams)
‚ Novon 7: 42. 1997. Cynan-
О. Williams, Fieldi-
. TYPE:
pas: steep slope x Dus. us along Mexican
Hwy. 190, 3 mi. S of La Trinitaria. alt. 5100
ft., 14 Oct. 1965, D. E. Breedlove & P. H. Ra-
ven 13199 (holotype, Fl: isotype, DS not seen).
Figures 14a-f. 15

iede & Mev
chum conan e
19

ana, Bot. 32: 37. Mexico. Chia-

Plants ascending: shoots perennial, basally

58 Annals of the
Missouri Botanical Garden

Yt ru
1005 D

Figure 13. Metastelma latifolium and Metastelma и a-f: Metastelma sie hic a: Palmer 665, b-f:

Steinman 955. a'-f': Metastelma minutiflorum, Gentry 4857. —а. Sho oot with inflorescence. —b, b'. Flow
Corolla lobe, adaxial view. —d. d', Gynostegium and corona, —e, e”. Pollinarium. f f'. Style-head. Drawn by J.

Conrad.

Volume 91, Number 1
2004

Liede & Meve 59
Revision of Metastelma

att

EE

(nr

=

ӨРЕ

1—7
— Zum

AVI
T

is
2

а
E

vs 7 " rj
qu "T

TM on
,

ДУ

Metastelma 2 oronatum.
. Pollinarium. —f.

Figure 14.
d. Gynostegium and corona

TEM re
IOS
d
DN

^

c
ا‎

1745
к

к view.

. Corolla lobe.

a. Shoot with inflorescences. —b. Flower. —
Stvle-head. Breedlove & Raven 13199. Drawn by J. Com

60

Annals of the
Missouri Botanical Garden

So — [1 | ¡PES
А E | | | | | P
el^, * | o 4
( | |
—— == E
7 | L— XA T
~a | €
AS | | lh {
PN К | 1—4 | |
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E A 31 WT
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QUT RN e
Е EN | | Е AY | E А A P [45 (^ А | Е س‎ а 7 20°
B Metastelma longicoronatum کی‎ з A К. WE A | J | ) 2
; A wt QUA SK M | Aj
e Metastelma palmeri ар , „
4 Matactal, f ; | n | S e e 1 y! * (
0 Metastelma turneri x M. pen NS eo — Sa 5 | ao |
„F EPIRI — = | < BUS: 15?
-120* -115* -110° -105° -100° -95° -90°
Figure 15. Distribution of Metastelma longicoronatum, M. palmeri, and M. turneri.
woody, with dark brownish bark, densely covered smooth, downward-directed trichomes, 150-200

along a single line with flexuous trichomes, 250—
300 um long; internodes 2—6 cm long, 1 mm diam.
Leaves with petioles 3-5 mm long, with 2 colleters
at blade base; blades 20-40 X 6-12 mm, ovate,
basally rounded, apically acute to acuminate, adax-
ially isolatedly covered mainly on veins and mar-
gins with appressed trichomes, 250—300 um long,
abaxially glabrous. Inflorescences always one per
node, 4- to 8-flowered, 3 to 5 flowers open syn-
chronously, sciadioidal; peduncles 3-15 mm long,
densely covered along a single line with flexuous
trichomes, 150—200 jum long; floral bracts 0.4—0.5

0.2—0.3 mm at the base, ovate, with trichomes
on the surface; pedicels 2-3 mm long, densely cov-
ered along a single line with recurved trichomes,
150-200 um long. Floral buds 2—2.2 mm long, 1—
1.2 mm diam., ovoid; calyx basally fused, campan-
ulate, abaxially with trichomes (mainly on the
tube); calyx lobes 0.8-1 X 0.4—0.5 mm, ovate, api-
cally acute; corolla campanulate, 2.5-3 mm long,
abaxially white, glabrous, adaxially white, with ver-
rucose trichomes, 100—150 um long, on the apical
and on the lateral parts of the lobes and with

шї long on the central parts of the lobes; lobes
basally fused to ca. % of total corolla length, ca. 1
mm wide, patent, ovate, apically acute, recurved;
gynostegial corona 2 mm long, longer than the gy-
nostegium; lobes erect, apically slightly connivent,
attached at the base of the stipe, laminar, elongat-
edly triangular and with a conspicuously winged
base. Gynostegium ca. 0.8 mm high, ca. 0.8 mm
diam., on a stipe ca. 0.6 mm long; anthers about as
high as broad, rectangular, abaxially planar; anther
wings 0.6 um long, extending along the entire
ength of the anther, anther wings of adjacent an-
thers parallel to each other, in the same plane as
the anther; connective appendages ca. 400 рт
long, ca. 300 um wide, ovate, narrower than the
stamen, slightly inflexed; pollinarium with corpus-
culum ca. 160 um long, more than twice as long
as broad, elliptic; caudicles ca. 70 jum long, flat-
tened, slightly s-shaped, concave-convex; pollinia
apically attached to the caudicles, ca. 180 jum long,
ca. 80 um wide, ovoid; style-head white, ca. 0.5

mm diam., ca. 0.4 mm high, upper part ca. 0.15

Volume 91, Number 1
004

Liede & Meve 61
Revision of Metastelma

mm high, shorter than the lower part. depressed-
conical. Follicles and seeds unknown.

Phenology. | Collected in flower in July. August,
and October.

Distribution. Mexico: Chiapas: cliff faces and
limestone bluffs with seasonal evergreen forest:
1300-1700 m.

Metastelma longicoronatum is a rare species en-
demic to Chiapas. The elongated triangular shape
of the corona lobes with a conspicuously winged,
almost hastate base, is unmistakable.

Additional specimens examined.

A Sumidera, 22 km ^ of |

. Breedlove 27183 (TEX); Comitán de Dominguez, 21
үч 1989 (fl). ад & Conrad 2557 (UBT).

MEXICO. € T
19

Tuxtla Gutiérrez, 19 Aug.

8. Metastelma mexicanum (Brandegee) Fish-
bein & R. A. Levin, Madroño 44: 270. 1997.

Basionym: Melinia mexicana Brandegee, Zoé

216. 1905.
degee) Bartlett, Proc.
632. 1909. TYPE:
E of Culiacan,

Basistelma mexicanum (Bran-
Acad. Sei. 44:
30 mi.
near Durango border, Cerro
3 Nov. 1904. J. S. Brandegee s.n
(holotype, GH not seen).

Amer.
Mexico. Sinaloa: ca

Colorado.
Figures З. 1ба—К.

. 1964. Bas-
Report on
159 59.

Cynanchum wigginsti Shinners, Sida 1: 36:
ionym: — ja Torr.
the U.S. & Mexica
non Metastelma angosta Turcz..
kovsk. Obsc. Isp. Otd. Biol. 25: 314. 1
Melinia —1 (Torn) A. Gray, Proc. Amer.

E Se i. 12: 73 dyra ê i

(Tor Watson 1 15 Amer. Acad. Sci 60.

1380. Basis oom re An ; Marte гос.

Acad. Arts 44: € : Mexico.

Sonora: Santa Cris; Tow = ane 2x holotype,
NY isotypes. GH!. MO not фм

1 Boundary Survey 2: 159. 1

Aca cl.
cal

Plants ascending. to 300 em high: subterranean
organs constituting a woody rootstock: shoots pe-
rennial. basally corky, densely covered along a sin-
200-250 um

long; internodes 2-3.5 cm long. 0.5—

gle line with recurved trichomes.
| mm diam.
Leaves with petioles 1-2 mm long, with 0 to 2 col-
leters at blade base: blades 20-40 X 1-2 mm, lin-
ear, basally cuneate, apically acute, marginally rev-
olute when dry. adaxially isolatedly to sparsely
covered on the midrib and the margins with re-
curved trichomes, 200—250 рли long, abaxially gla-
brous. Inflorescences always one per node. 2- to
A-flowered, all flowers open synchronously, scia-
dioidal; peduncles 0-2 mm long. densely covered
along a single line with recurved trichomes, 150-
200 um long: floral bracts 2-3 * 0.2-0.3 mm at
with trichomes

the base. very elongate triangular.

on the surface: pedicels 2-3 mm long. densely cov-

ered along a single line with recurved trichomes,
150-200 um long. Floral buds ca. 3 mm long. ca
1.5 mm diam., ovoid; calyx basally fused:

lobes 2.2-3

angular,

calvx
0.3—0.4 mm, very elongatedly tri-
apically acute, abaxially with recurved tri-
chomes: corolla campanulate, 2.5-3.5 mm long.
abaxially white, glabrous, adaxially white, adaxially
with verrucose trichomes to 50 jum long on the api-
cal parts of the lobes and with smooth trichomes,
150 pm long, forming a tuft at the entrance of the
tube; lobes basally fused, ca. 1 mm wide, patent.
ovate, apically acute, recurved; gynostegial corona
ca. 1.2 mm long, shorter than the gynostegium:
lobes erect, attached at the base of the stipe. at-
tached with a distinct hook-shaped base, laminar,
obovate. Gynostegium 1.4-1.6 mm high, 1—1.2 mm
diam.. on a stipe 0.4 mm long: anthers broader than
high. deltoid, abaxially planar; anther wings 300—
100 um long. extending along the entire length of
the anther, anther wings of adjacent anthers par-
allel to each other, in the same plane as the anther:
connective appendages 900-1000 um long, 400—
500 pm wide, ovate, narrower than the stamen.
erect; pollinarium with corpusculum ca. 300 рт
long. more than twice as long as broad. elliptic:

caudicles ca. 150 jum long, flattened, convexly re-

curved, horizontal. ellipsoid-rectangular: pollinia
subapically attached to the caudicles, ca. 300 jum

long. ca. 150 um wide, ovate in cross section, ob-
longoid; style-head white. ca. 0.8 mm diam.. ca. 1.2
mm high, upper part ca. 0.8 mm high. longer than
the lower part, elongated-conical to obinfundibuli-
Follicles 50-60 mm

long, 4—5 mm diam.. obtusely deltate in

form. one per flower. erect.
fusiform,
cross section, apically strongly beaked, medium
light

brown, seta side tuberculate, papillose with regu-

brown, longitudinally grooved: seeds ovale.
larly arranged papillae, aseta side sculptured with
longitudinal ridges, with regularly arranged. papil-
lae, marginally wingless, denticulate: coma 10-15
mm long.
Phenology. Collected in flower from June to
August and in October; in fruit in October.
Distribution. Mexico: Sonora; U.S.A.: Arizona,
New Mexico; open rocky slopes in eni wood-
lands, tropical deciduous forest: 900-1550 m.
Metastelma mexicanum is probably the most dis-
tinctive Metastelma species in the southwestern
U.S.A. and Central America. It possesses extremely

large sepals reaching the length of the corolla ii

—

some specimens (e. g., Jenkins 93-88, ARIZ). The
corona is basally fused to the stipe but also to the
corolla base. a character shared only with a few
South American Metastelma species (e.g.. M. par-

62 Annals of the
Missouri Botanical Garden

Figure 16. Metastelma mexicanum. —a. Habit. —b. Inflorescence. —c. Flower. —d. Sinus of corolla lobes, abaxial
view, е. Two corolla lobes and one corona lobe, adaxial view. —f. Gy 5 E Pollinarium. —h. Style-head.

‚ Follic le. —j. Seed. a-h: Spellenberg & Repass 5353. i-k: Van Dann et al. s.n. Drawn by J. Conrad

Volume 91, Number 1
2004

Liede & Meve 63
Revision of Metastelma

viflorum, see introduction). Most diagnostic. how-
ever, are the large. erect anther appendages. which
are nearly as long as the elongated stvle-head. For
a discussion of infraspecific variation, see Fishbein
and Levin (1997)

canum is probably М. arizonicum, judging from gy-

The closest relative of M. mexi-

nostegium structure.

=
Е

\dditional specimens examined. MEXICO. Sonora:
Sierra 5 оле road from Saguaribo to El Chiribo
23 Aug. 1993 ( Fishbein et al. 1362 ( а
Т Mesa E ssopaco, above La Vinateria. ca. 35 К
Alamos, 1275 m. 24 Aug. 1993, Fishbein el al.
j ARIZ): ridge SW of Santa Barbara, 20 air mi. ENE
1450 m. 3 June 1993, ogi = 88 (ARIZ):

Sierra

| 148
of \lamos.

Sierra de Alamos. ca. 900 m. 19 Aug. Steinmann
s.n. (ARIZ): Palm Canyon, 17.7 mi.“ = и е in
Cerro € inta de Plat side 1976. Van е et al.
s.n. (ARI ca. | 200 m. ban n & $
(ARIZ). e D 1971. Van alios Goldberg & "Turner
s.n. (ARIZ). U.S.A. New Mexico: Hidalgo Co.. Guade-

lupe a. 16 Aug. 1979, Spellenberg & Repass 5355
Y

9. Metastelma minutiflorum Wiggins. Contr.

Dudley Herb. 3: 71. 1940. elec: sono-

rense Moran. in Levin & Moran. Vasc. Fl. Isla
Socorro, Mexico (Mem. San Diego Soc. Nat.
Hist. 16): 26. 1989, non C. minutiflorum N.
Schum.. Nat. Pflanzenfam. 4(2): 1895.
TYPE: Mexico. Sonora: hills between Magda-

lena and Santa Ana. 7 mi. S of Magdalena. 14
Sep. 1934. J. L. Wiggins 7191 (holotype, DS

not seen: isotype, USD. Figures 10. 134—£,
Plants ascending. to 150 em high: shoots basally

woody, with brownish bark. densely covered along

two lines with recurved trichomes, 150-250 um
long: internodes 2.5-5 em long. 1-1.5 mm diam.
Leaves with petioles 5-6 mm long. with 1 or 2 col-
(10—)20—50 × 3—5 mm.

acute.

leters at blade base: blades
narrowly ovate or narrowly obovate. basally
apically acute, adaxially sparsely covered on the
midrib and the margins with flexuous trichomes,
250—300 um long, abaxially glabrous. /nflorescenc-
es always one per node, 3- to 6-flowered. all flowers
open synchronously, sciadioidal, subsessile: floral
bracts 0.4—0.5 X 0.2-0.3 mm at the base.
gular to ovate: pedicels 1—1.2 mm long. isolatedly

trian-

covered over the entire surface with appressed tri-

chomes, 140-200 um long. Floral buds ca. 1.5 mm

long. ca. 1 mm diam., ovoid: calyx basally fused,

campanulate, abaxially glandular. ot with
sparse trichomes: calyx lobes 1— ).3-0.4

mm. ovale, apically acute: corolla ыен

7-2 mm long. abaxially cream, glabrous, adaxi-

ally 150—

long. on the apical and on the lateral parts of the

white. with smooth trichomes, 250 um

lobes: lobes basally fused, 0.5-0.6 mm wide. patent
to incurved, ovate, apically acute: gynostegial co-
гопа 0.6—0.7 mm long, shorter than to equaling the
eynostegium: lobes erect, attached directly under-
neath the anthers, laminar, lanceolate. Gynostegium
0.7-0.9 mm high.

anthers about as high as broad.

0.7-0.9 mm diam.. subsessile:
rectangular, abax-
ially planar: anther wings 0.4-0.5 um long. ex-
tending along the entire length of the anther, anther
wings of adjacent anthers parallel to each other. in
the same plane as the anther: connective append-
ages 300-350 um long. 200-250 um wide. obcor-
date. equaling the stamen in width, slightly in-
flexed: pollinarium with corpusculum. 75-80 pm
long: caudicles 50 jum long. cylindrical. s-shaped.
convex-concave, thickened at the insertion of the
pollinium: pollinia apically attached to the caudi-
cles. 75 um long. 50 um wide, ovate in cross sec-
tion. reniform: style-head white, 0.3-0.4 mm diam..
0.1—0.5 mm high. upper part 1.5-1.7 mm high.
shorter to equaling the lower part. conical to knob-
by. Follicles one per flower. 60-75 mm long. 4-5

mm diam.. fusiform, terete, apically strongly
beaked. blackish brown. glabrous: seeds 5-6 mm

long. 3-3.5 mm wide, pyriform. seta and aseta side
tuberculate. papillose with regularly arranged. pa-
pillae. marginally wingless, denticulate: coma 15-
20 mm long.

Phenology. Collected in flower in April. Sep-
tember, and November: in fruit in November.
Distribution.

thornserub and grassland:

Baja California, Sonora:
200—500 m.
Wiggins (1940: 82.

Mexico:

Literature and illustrations.
17

pl. ij.

Cynanchum minutiflorum is a name not available
for this taxon. because it is preceded by Cynan-
chum minutiflorum K. Schum.. Nat.
4(2): 252. 1895, today considered a synonym of C.
schistoglossum Schltr. (Liede. 1996b). Under Me-
Metastelma minutiflorum is

Pflanzenfam.

tastelma, however,

available and thus valid. For comments on a close

relationship, see M. latifolium.

Additional specimens e pow MEXICO. Baja Cal-
ifornia Sur: canyon of W slope of peak ove кеч salt-
Apr. 1962 (f. Moran 9141
Nov. (f), Gentry 4857 (NY, TEX): Yecora,
1998 n Tr Devender et al. 98-1285 (ARIZ).
10. Metastelma palmeri S. Watson. Proc. Amer.
Acad. Arts 18: 115. 1883. Cynanchum gravi
Shinners, Field & Lab. 20: 110. 1952.
maccartil,

Cynan-
chum maccartii Shinners var. Sida
: 360. 1964. nom. nov. for Cynanchum pal-

meri (S. Watson) Shinners. Field & Lab. 19:

64 Annals of the
Missouri Botanical Garden

„% UY
AA
NOM ip
ПОЛ

0.5mm
а m ey чаш palmeri. 1. Shoot e inflorescence. —b. Inflorescence. —c. Flower. —d. Corolla кё.
adaxial у ynostegium and corona. —f. Pollinarium. —g. Style-head. a: E 828. b. Pringle 6706.

Liede & ыш 2612. Drawn by J. Conrad.

65. 1951, non Cynanchum palmeri (S. Watson) Metastelma macropodum Greenm., € Amer. Acad. Arts
181. 1898. Syr YP

Blake, Contr. Gray Herb. 52: 83. 1951. TYPE: 33: 481. 1898. Syn. nov. TYPE: Mexico. Oaxaca:

. . E . | Tomellín Canyon, 1540 m, 17 s 1897, C. G. Prin-
U.S.A. Texas: Webb Co., Laredo on the Rio gle 7606 (holotype, NY!: isotypes, HBG!, M!, MO
Grande, Aug. 1879, E. Palmer 824 (lectotype. not seen, Pl. SN.

designated by Henrickson (1987: 98), GH not
seen; isotype, NY!). Figure 17a-g. Plants ascending, 50-200(—400) cm high: sub-

Volume 91, Number 1
2004

Liede & Meve 65
Revision of Metastelma

terranean organs constituting a woody rootstock:
shoots perennial, basally slightly woody. with vel-
lowish brown to blackish bark. glabrous, isolatedly
sparsely covered along a single line with re-

200—300 um long:

mm diam.

curved to flexuous trichomes,
internodes 2—4 cm long. ca. | Leaves
with petioles 2-7 mm long. with 2 colleters at blade
blades (12>)16-35(255) X 2.5
ovate, basally rounded, apically acute, marginally

base: —((-12) mm.
revolute (when dry), adaxially isolatedly to sparsely
covered, mainly or only on the midvein with ap-
pressed to recurved trichomes, 150-250 pm long.
abaxially glabrous. Inflorescences ен опе рег
3- to 8-flowered, 2
open synchronously, thyrsoidal to setadioidal: pe-

node, extra-axillary, 2 to 6 flowers
duncles 0-10 mm long. densely covered along a
single line with recurved to flexuous trichomes.
150-200 um long: floral bracts 0.4—0.7 * 0.2-0.5
mm at the base, triangular, glabrous: pedicels 0—5
mm long, glabrous or isolatedly to densely covered
200—
250 um long. Floral buds 1.5-2 mm long. 0.8-1.5

along a single line with recurved trichomes,

mm diam., ovoid: calyx basally fused. campanulate.
abaxially glabrous or with a few sparse trichomes
lobes 0.5-1.3 X 0.2-0.5 mm. ovate.

apically acute to obtuse: corolla campanulate. 2.2—

on the tube:

J

3 mm long, abaxially white to cream, glabrous.
adaxially white to cream, with smooth trichomes.
100(—150) рт long, on the apical and on the lateral
parts of the lobes, apical trichomes not longer than
lateral ones. and deflexed hispid trichomes on the
central parts of the lobes: lobes basally fused, 0.0—
| mm wide, patent, ovate, apically acute, recurved:
gynostegial corona 0.7—1 mm long. equaling to lon-
ger than the gynostegium:; lobes erect to inflexed.
attached directly underneath the anthers, laminar.
ovale to triangular. Gynostegium 0.4—0.7 mm high.
0.5-0.8 mm diam.. on a stipe 0.3-0.4 mm long:
anthers about as high as broad, trapezoidal, abax-
ially planar: anther wings 200-250 pm long. ex-
tending along the entire length of the anther, the
stamen forming a basal arch: anther wings of ad-
jacent anthers parallel to each other, centrifugal.
basally forming a distinct “mouth”: connective ap-
pendages 200-250 um long. 250—300 um wide.
ovale. narrower than the stamen. slightly inflexed:
pollinarium with corpusculum. 100—150 um long.
between 1.5 times and twice as long as broad, ovoid
to elliptic: caudicles 50-70 um long. cylindrical.
shaped. convex-concave: pollinia apically at-
tached to the eaudicles. 120—150 рт long. ca. 50
um wide, ovate in cross section, oblongoid: style-
—0.3 mm high.
upper part 0.05—0.1 mm high, shorter than the low-

head white. 0.4-0.5 mm diam.. 0.2

part, depressed-conical to umbonate. Follicles

one per flower, 40-60 mm long, 4.5-5.5 mm diam..
i dark

brown, glabrous; seeds 6—7 mm long, 3—4 mm wide,

fusiform, terete, apically strongly beaked.

ovate, medium brown, seta and aseta side smooth.
marginally with 0.1—0.2 mm wide wing with entire
margin.

Phenology. Collected in flower from July to Oc-
tober; in fruit in August.

Distribution. Guatemala: Izabal: Mexico: Coa-
huila, Nuevo León, Oaxaca, Puebla, Tamaulipas, Yu-
catán; U.S.A.: Texas: on limestone, but also on ig-
neous rock, matorral and thorn forest; 500-2000 т.

Literature and illustrations. Henrickson (1987:
98, fig.

Apparently, the same author published two re-
placement names for Cynanchum palmeri, Cynan-
chum grayi (Shinners, 1952) and Cynanchum mac-
cartii 1964).

the intentions of Shinners (1952, 1964) in both cas-

(Shinners, As there is no doubt about
es. and Cynanchum grayi would have been a name
available for the taxon, an error is the most prob-
able cause for this duplication. Henrickson (1987)
remedied the situation by designating the same lec-
totvpe for M. palmeri and С. maccartit.
9.336
9319 from the Yucatán Peninsula. both out of the

Contreras from Guatemala and Conrad
main distribution area in Mexico, display a corona
a little more stout than usual, but are best accom-
modated here until more material from this area
vecomes available.

The

name applied to collections from central Mexico.

specimens of Metastelma macropoda, .

are indistinguishable from those of M. palmert. and

M.

M. macropoda is thus placed in synonymy of
palmert.

The flowers in the Metastelma palmeri complex
are easily confused with those of M. minutiflorum
and M. latiflorum. which show a very similar struc-
M. latifolium and M. minutiflorum
occur along the Pacific slope, while M. palmeri oc-

ture. However.
curs along the Gulf Coast. Morphologically, M. pal-
meri can be distinguished by slightly larger flowers
(corolla 2-3 mm long on average in contrast to less
than 2 mm in M. latifolium and M. minutiflorum).
broader and longer corona lobes (basally as broad
as the anthers, and as long as or slightly longer than
the gynostegium in contrast to smaller than the an-
thers throughout and never exceeding the. gynos-
tegium in M. latifolium and M. minutiflorum). and
a more clearly stipitate gvnostegium. Most conspic-
uous. though only visible under a dissecting micro-
scope, are the very tiny pollinarta (120-150 X ca.
50 pm) with their thin and fragile caudicles.

GUATEMALA. Iza-

pr

dditional specimens examined.

Annals of the
Missouri Botanical Garden

bal: Cadenas (Puerto Mendez), 13 Oct. 1969 (fl), Con-

treras 9336 (LL, NY). MEXICO. hog ge Canyon la

yavia, in N side of Sierra de la Gavia, 2 Aug. 1973 (fl,

fr), Henrickson 11724 (TEX): Catacol Mis. Aug. 1880 (fl),

Palmer 828 (NY); 22 km ESE of La Cuesta del Plomo on

the 2 اا‎ Boquillas Hwy., 7 June 1972 (fl), Chiang et
0 (NY, TE

~

al. 755 TEX): € че nda Mariposa, at the foot of the
реА rn slope of the та de Puerto Santa Ana, 23 June
1936 (fl), Wynd & Ы pee (ARIZ, NY, WIS); Múz-
Men Palm Canyon, 7 аси 1936 (tl). Marsh 305 (TEX):
Rancho Las Tres Sabinas ca. 15 m. de Músquiz, 5 June

72 (f), Chiang et al. 7527A (T ; Rincón de Maria,

24 Aug. 1975 (fl), Wendt et al. 1328 155 ; Hwy. 57, 70
mi. N of Sails, 3 June 19 66 (fl), Wilson 11. 388 (TEX).
Nuevo León: Mts. Bustamante, Aug. 1938 (fl),
LeSueur 361 (TEX); Old Pasa road, Paso de O
8 pan 1989 (fl), Liede & Conrad 2612 (UBT). Oaxaca:
Concepción qe sta, base del Cerro Pluma, Santa Lu-
cia, 4 July 1994 (fl), Panero & Calzada 4026 (LL); distr.
Huajuapan, 15 km al o de 55 13 July 1986
(fl), Mendoza & Mérida 2566 (LL); eforma entre Hua
juapan de León y Meere 6 pe Pr 5 (fl). ou
& Garcia 6656 (LL). Puebla: a Los Gri inea ca. 20
km al O de n 24 Sep. I 990 m тте 5790 (NY):
ear Oaxaca, cerro de Costapa near San Luis Tultitlanapa,
June 1908 (ib. Purpus 3244 (NY). agire 4.4 mi.
NE of turnoff to биши, оп a ias
(f), Nesom et al. 5957 (LL); Carretera eh
vs 8 mi. 5 of "alm. 20 July ans (0), КО?
TEX); along Hwy. 85, . М over rive
brider at Colonia 1 1976 (fl). Stevens et
al. 2260 (NY); 37 mi. out of Re eynosa on the 15 to San
Fernando, 19 Oct. 1959 (fl), Johnston 4369 (TEX); near
microwave tower above Villagran, 30 ded vlr (fb. : Ste-
. Park, са
5 km N Celesttin, 16 May 1993, Conrad s (U BT),
A. Texas: Brewster Co., end of trail down from Mt.
1 155 to camp in Basin, 2 Sep. 1947 (fl), ae 4088
(NY); Je ous Davis Co., Point of Rock on Ft. Davis—
Valentine Hwy., 27 July 1947 (fl), Hinckley Pu A
Live Oak Co.. Toad to Fiesta Marina just E of Rte. 534,
1.6 mi. N of Rte. 359, 26 July 1981 (f). Hill Da 7 (NY)

11. Metastelma pedunculare Decne., in A. P. de
Prodr. 8: 1844. Cynanchum
w woodsonianum L. О. Williams, Fieldiana, Bot.
: 12. 1968, non Cynanchum pedunculare
T 1786. TYPE: Guatemala. Cuesta de Piñ-
ula, 1837, K. T. Hartweg 601 (holotype, G not
seen; isotypes, NY—2!, P!). Figures 12, 18a-f.

Candolle,

ки vse ola Pittier, Contr. U.S. Natl. Herb. 13: 98.

910. Cynane ir ۰ ittier) L. O. Williams,
En Bot. . TYPE: C osta Rica. San
José: July pe " indue s.n. (holotype, US!; iso-
type, P!)

Plants ascending: shoots perennial,
woody, with grayish bark, glabrous. Leaves with pet-
ioles 4—7 mm long, with 0 to 2 colleters at blade
base; blades 25-60 x basally
rounded, apically acute to acuminate, adaxially gla-

basally

7-17 mm, ovate,

brous or sparsely covered only on the midvein with

recurved trichomes, 300-400 um long. abaxially

floral bracts 0.3-0.4 X

glabrous. Inflorescences always one per node, 6- to
8-flowered, one specimen more than 15- to 20-flow-
ered (Molina 23080), 1 to 3 flowers open synchro-
nously, bostrychoid: peduncles 10-25 mm long,
densely covered along a single line with recurved
trichomes, 100—150 um long; rachis 0-2 mm long,
straight or 3—17 mm long, angular (Molina 23080);
са. 0.2 mm at the base,
triangular, ciliate; pedicels 3—5 mm long. glabrous.
Floral buds 1.5-2.5 1-1.5 mm diam.,
ovoid: calyx basally fused, campanulate, abaxially
glabrous, ciliate or with very few trichomes; calyx
lobes ca. 0.6 X ca. 0.3 mm, ovate, apically acute;
campanulate, 2-3.5 mm long, abaxially
cream, glabrous, adaxially creamish white, with
verrucose trichomes, 100—150 um long. on the lat-
eral parts of the lobes; lobes fused for ca. % of total
mm wide, horizontal to re-

mm long,

corolla

corolla length, са. 0.7
curved, ovate, apically acute; gynostegial corona
0.5-0.6 mm long, equaling the gynostegium; lobes
inflexed, attached directly underneath the anthers,
laminar, oblong. Gynostegium 0.3-0.5 mm high,
0.6-1 mm diam., on a column 0.6-1 mm long or
only 0.3 mm long (Molina 23080); ie broader
than high. rectangular, abaxially planar; anther
wings 200—250 um long, extending along the entire
length of the anther, anther wings of adjacent an-
thers parallel to each other, in the same plane as
the anther; connective appendages ca. 250 um
long. ca. 250 um wide, ovate, narrower than the
stamen, strongly inflexed; pollinarium with corpus-
culum ca. 200 jum long, more than twice as long
as broad, elliptic; caudicles ca. 150 jum long, ey-
lindrical, s-shaped, convex-concave; pollinia ca.
75

200 um long, ca. 75 um wide, ovate in cross sec-
tion, clavate; style-head white, 0.6-1 mm diam.,
0.2-0.3 mm high, upper part flat. Follicles and

seeds not seen, follicles 45 mm long (fide Standley,

2

Phenology. Collected in flower in July, August,
and November.

Distribution. Costa Rica: Cartago,
Guatemala: Guatemala; Nicaragua: Estelí; volcanic
soil, in ravines, thickets, along borders of fields:
1000-1800 m.

Literature and illustrations.
fig. 5)

Specimens from Guatemala and Costa Rica show
no constant differing characters, as Standley
(1938b) observed correctly. He (Standley, 1938b)
placed Metastelma sepicola in synonymy of M. pe-

San José;

Pittier (1910: 97,

dunculare.
In Metastelma pedunculare an exceptionally long
and slender column (to 1 mm) carries the short and

Volume 91, Number 1 Liede & Meve 67
2004 Revision of Metastelma

С

0

y
3 b,

Figure 18. Metastelma pedunculare. —a, a’, a". Shoot with inflore scence. ==”. Inflorescence. с. e”. Flower. =
d. Corolla lobes, s view. n X Gynostegium and corona. —e - Pollinarium. —f, f'. Style-he ad. a-f: Specimens
from Guatemala. a: Hartw 8, 601. : Molina & Molina 24843. a. A: Specimens from Costa Rica. a^: Tonduz s.n. b'—
P: Taylor & Taslor 11393. a", b”: ы imen from Nicaragua, Mattia 23080. Drawn by J. Conrad.

68

Annals of the
Missouri Botanical Garden

flat gynostegium. The short laminar corona lobes
are inserted directly beneath the anthers and are
curved along the back of the anthers in a hook-like
manner. In M. stenomeres, the only other highly
stipitate species with the corona lobes inserted di-
rectly underneath the gynostegium, the corona
lobes are much longer than the gynostegium, while

they barely exceed it in М. pedunculare.

Molina 23080 from Nicaragua, a specimen cited

by Stevens (2001) as representative of Metastelma
species "B," is easily identified by its bostrychoid
inflorescences, which are, however, more richly
branched than in other specimens. Also, compared
to material from Guatemala and Costa Rica, the
stipe and the corolla tube are quite short. However,
gynostegium and corona structure agree well with
M. pedunculare, so Molina 23080 is included here
until more material becomes available from which
it can be judged whether the characters described
for Molina 23080 are typical for Nicaraguan ma-
terial and can be used to circumscribe a subspecies
of М. pedunculare.

Additional specimens examined. COSTA RICA. Car-
go: 3 km SE of 5 11 Aug. 1967 (fl), Taylor cae
(NY), 4285 (NY). Pur xe о Guacimal valley,
Oct. 1984 (fl), Haber 575 5 "Т. L, WIS). San José: about :
km NW of San Juan de Tibas song the Rio Virillo, 1 Aug.
=e (9), 1 М е 11393 (NY); entre Frailes y La
1, 26 Nov. » (fl), ins 2617 (NY ^ Acosta, En-
Pg 97.18 (U a GUATEMA yala: 7 km E
of Guatemala City, 24 "e 1970 (fl), o 4189 (NY);
betw. km 18 to 22 on Hwy. from Guatemala City to An-
i Molina & T na 24843 (NY).

>

NICAR stelí: don › Estanzuela Creek, 8 km W
of Estelf, 4 Nov. 1968 (fl), Molina 23080 (NY).
12. Metastelma пш А. ‚ Ргос. Ашег.

Acad. Arts 21: 396. 1886. "s ynanc iin Lak Sai
(A. Gray) cd rA 12: 91. 1987. TY
Mexico. Chihuahua: near Chihuahua, 23 May
1885, C. G. Pringle 62 (holotype, GH not seen;
isotype, US!). Figures 19a—f, 20

d.

—

кше iue isi (Scheele) Shinners var. breviflo-

1 S. Sida 1: 360. 1964. TYPE: U.S.A. Tex-

as: wster Co., Big Bend oe Park, Chisos

18., 1800 m, 19 July 1952. G. L. Webster 4340
(holotype, SMU not seen).

100—400 cm
high; subterranean organs constituting a woody
rootstock (Hinckley 2105, 3106); shoots perennial,
basally slightly woody, with yellowish brown or
grayish bark,

Plants ascending to decumbent,

rarely glabrous, normally sparsely
covered along a single thin line with recurved tri-
150-250 um long: 1-4 cm
long, | mm diam. (green shoots) or 2-3 mm diam.
(woody parts). Leaves with petioles 2-5 mm long,

chomes, internodes

with 1 or 2 colleters at blade base; blades 10—20(—
30) X 2-10 mm, ovate to elliptic, basally rounded,
apically acute, marginally revolute (when dried),
adaxially glabrous (except for a few isolated tri-
chomes on midvein and the margin). abaxially gla-
brous. Inflorescences 2- to 6(to 12)-flowered, 2 to 6
flowers open synchronously, sciadioidal; peduncles
0—2 mm long, densely covered along a single thick
line with recurved trichomes, 150-250 рт long:
floral bracts 0.6-1.2 X 0.3-0.6 mm at the base,
triangular, glabrous; pedicels 1.2-2.5(—4) mm long,
glabrous, sparsely covered along a single line with
recurved trichomes, ca. 200 jum long. Floral buds
calyx
basally fused, abaxially glabrous; calyx lobes 1—1.2

X 0.4—0.5 mm, ovate, apically acute; corolla cam-

2.3-3 mm long, ca. 1.5 mm diam., ovoid:

panulate, 2.8—4 mm long, abaxially white or yellow
to brown (when dry), glabrous, adaxially white, with
slightly verrucose trichomes, 200—700 um long, on
the lateral and apical parts of the lobes, apically
very long and wavy, and with hispid retrorse hairs,
300—500 um long, on the central parts of the lobes;
lobes fused for ca. % of total corolla length, 0.7—
1.2 mm wide, patent, oblong to lanceolate, apically
thickened, acute, with straight thickened margins:
gynostegial corona 1.3-1.8 mm long, twice as long
as the gynostegium; lobes erect, attached at the
base of the stipe, solid to filiform, subulate, ex-
tended into a long, slender tip. often incurled or
coiled. Gynostegium 0.5-0.7 mm high, ca. 0.7 mm
diam., on a stipe 0.5-0.7 mm long; anthers broader
than high.
wings ca. 250 jum long, extending along the entire

trapezoidal, abaxially planar; anther
length of the anther, anther wings of adjacent an-
thers parallel to each other, centrifugal; connective
appendages 200-300 um long, 200-300 jum wide,
ovate, narrower than the stamen, slightly inflexed;
180 um long,
more than twice as long as broad, elliptic; caudicles
ca. 50 um long, cylindrical, geniculate, thickened
at the insertion of the pollinium; pollinia apically

pollinarium with corpusculum ca.

attached to the caudicles, ca. 200 jum long, ca. 8

um wide, ovate in cross section, ovoid; style-head
white to cream, ca. 0.6 mm diam., ca. 0.5 mm high,
upper part ca. 1.6 mm high, shorter than the lower
part, depressed-conical. Follicles one per flower,
40-62 mm long, ca. 5 mm diam., obclavate to fu-
siform, apically strongly beaked, dark
brown, glabrous; seeds 5-6 mm long, 2.5-3 mm

terete,

wide, ovate, reddish light brown, seta and aseta
side smooth, marginally with 3 mm wide wing with
entire margin; coma 20-25 mm long.

Phenology. Collected in flower from May to Oc-
tober; in fruit in April, and from June to October.

Volume 91, Number Liede & Meve 69
04 Revision of Metastelma

,

7 SAAN Hub

NAH

SUN

N

M

CN

МММ

SS

SS

SSS
—

SSA
Se

— ey

— |
0.2 mm

м

=
` ===
SE

—

—

aa
—

—

—c. Corolla lobe. adaxial view. —d.

Metastelma pringlei. —a. Shoot with inflorescences. —b. Flower.
inarium. —f. Style-head. a-f: Pringle 62. Drawn by J. Conrad.

Figure 19

g 1
'stegium and corona. —e. Poll

Gyn

70 Annals of the
Missouri Botanical Garden
| | T ;
| | E:
N | — | | | (C)
Ke Й m~- | D
E AN | | |
i | }
X — — po H p 35°
| | | | | [AMA T |
` \ hi D Р | | à |
| | | | |
А ) |
1 | к 1] |
IN ) 1 | | A
\ \ { Li Јљ Фа
i k ! 15 Re 30°
V A у
|. 4
| v4 *
N v.
— 1 25°
| ry
ү | E. 20*
e Metastelma pringlei 7
" A
А Metastelma schaffneri m mo
EI 4
Гы» o
— Pe 15°
- |
-120° -115° -110° -105° -100° -95° -90°

Figure 20. Distribution of Metastelma pringlei and M.

Distribution. Mexico: Chihuahua, Coahuila,
Durango, Nuevo León, San Luis Potosí, Tamaulipas,
Zacatecas; U.S.A.:
gypsum and lava, matorral, open pine forest, scrub,
roadsides; 500-2300 m.
Literature and illustrations.
82); Henrickson (1987: 93, fig.
The impressive crown formed by the long (to 1.8
mm), erect and often incurled corona lobes makes
Metastelma pringlei an easily recognized species.
The corolla indumentum with two different types of
the conical gynostegium and the caudicles,

Texas; rocky slopes, limestone,

Wiggins (1940:

C-).

hairs,
which are apically inserted to the conical pollinia
via a thickened, convex area, demonstrate its close
relationship to M. barbigerum (cf. Fig. la, b). Shin-
ners (1964) even described U.S. material of M.
pringlei as a variety under М. barbigerum. How-
ever, the two species are easily and consistently
separable by the corona lobes ca. twice as long as
the gynostegium in M. pringlei (less than 1.5
as long in M. barbigerum). Only one specimen has
been found that is possibly a hybrid between the
two species (Mexico. Coahuila: 13 mi. S of Sabinas,
23 Aug. 1938, Shreve 8417, ARIZ). It displays the

times

schaffneri.

slender leaves of M. pringlei in combination with a
corona a little longer, but not twice as as long as
the gynostegium and the bearded corolla lobes typ-
ical for M. barbigerum subsp. barbigerum.
Additional specimens examined. MEXICO. Chihua-
hua: 4 km SSW of Cerro del Gringo in the Sierra del
Diabolo, 30 Aug. 1972, Chiang et al. 9015f (TEX); hills
near Chihuahua, 5 Sep. 1886, Pringle 955 (NY); Mts. NW
of Chihuahua, 1 Aug. 1936, te ur 1053 (TEX); Santa
Eulalia Mts., 1885, Pringle 70 (N Deis Sierra de la
Campana, Rancho La Campana, 5 n 1977. Socorro
Gonzales 840 (TEX): S slope & top of Sierra del Roque,
NNE of Че 19 June 1973, Chic pida el ER 11387
(TEX): c l (air) mi. NE of с SW f
above ee el Recuerdo in Sie
1973. Henrickson 12980b (TEX). Coahuila: Arroyo Seco,
en el ‘ho el Tunal entre las Sierras San José y El Tunal,
E de Parras de la Fuente, 14 Aug. 1983 (fl), .
Rodriguez & Carranza 1111 (ARIZ, LL); ca. 12 (air)
E of Boquillas in Sierra del RUM 10.4 (rd.) mi. NW of
Rancho El Jardin, 27 July 1973 (fl). Henrickson 11497
(LL); Cañon San Lorenzo, SE d Saltillo, 2 Aug. 1975 (fl).
Engard & Gentry 686 (LL); Canyon de Tinaja Banca, cen-
tral mass of Sierra de las Curces W of Santa Elena
14 Aug. jme ). Johnston & Muller 261 (TEX); ien 6.9
1. SW of Cuatro Ciénegas on Hwy. to San Pedro, 27 Sep.
1986 (H. fr), pene 20400 (LL); 8 km W Vy MM

Volume 91, Number 1
2004

Liede & Meve TA
Revision of Metastelma

Ciénagas, slopes of Sierra de la he га, 5 Aug. 1973 (fl).
Ги et al. 12077 (NY. TEX): 35 (air) mi. W of
in pe Canyon del la Шаш

3 (fl). Henrickson & дйн, 1202 28

Cuatro Ciénegas,
de la Madera, 6 Aug.

(LL): ca. 43 (air) mi. D of Cuatro Ciénegas, 4 mi. SW of
Hacie ada Zacatosa, 7 Aug. 1973 (fl). He aki 12070
(LE) 52 mi. WNW of Cuatro Ciénegas (12 mi. E of La
Vibora). 20 Sep. 1972. Henrickson 7891 (LL): ca. 07 (air)

mi. SW of Cuatro Ci iénegas, above the main spring. 1.5
Ў, 15 Aug. 1973 (fl. fr). Henrickson
. NW of | as Delicias, valle "V
of Sierra «
Е "nrickson E = Ly
N of Ejido Piedritas, 12 5 Sep. 1972 e Chiang. et al.
930604 (NY) J: rd. from Esmeralda NE to San /
s (via Mans and Emple us | Sep. 1940 (fl),
Vim 4 Muller 834 (LL); 4 km E of Fraile, 12 July
a ea E ер 362 (ARIZ. NY): E of Hacienda
p Б l4 Jur 936 (fl), Wynd & Mueller 26 (ARIZ,
NY): 11 km "E ч is и June 1941 (fl). Stanford et
» km NNE of Las Margaritas in a large
canvon E face i "ierra de = Е 24 Sep. 1972
(D. Chiang et al. 9501 (LE): c La Morada Ranch, 2

m.

. Hinton 23343 (TEX): W base of Picacho del
ида Vaione па. 23 Aug. 1941

; Pore ‘ion Y W de la sierra la bap а ca. 45

a Carito Giz ey s. 5 Apr.
Bounty et al. 17 (LL): Puerto de
1. fn: fous & Van Devender 9239 (ARIZ); SW
flank of Sierra del Carmen, 15 Sep. 1972 (1). Chiang е!
A 9274 (LL): 1.5 mi. S of Rte. 40 on road ph canyon,
нар TAA rd. and Rte. 5 Aug.
(LL): vicinity of im ho El
е № a Y deed & close to the Chi-

1130 m Los re : 28 July
(fl), Vilaseñor et al. 1621 (LL); N de of iit de la Fra-
gua, E of Estacion Belloc, 38 km W of € uatro Ciénegas,
19 Oct. 1985 0» La vin et al. s.n. (LL); <
Antonio, сапу‹ Antonio de los 2 Sep:
1940 (M. Johnston & Muller 950 ba L): Sierra de Parras.
ca. 18 km S de Parras de la Fuente. 14 Oct. 1983 (fl, fr).
Rodriguez 1024 ( ARIZ): Sierra San Marcos. W of Revn-
olds Mine He quate rs, и Colorado turnoff W of San
2 July 1974 (fl). Engard. & Getz

azaro Pass, Hwy. 57

Cienagas,
(ARIZ); lower canyon & Mim e ES rra San Marcos op-
posite Laguna Grande, 14 Aug. 5 (1). Reeves & Pin-
kava 13075 (NY): S ih of Sierra Lus y Organos, ca. 9.5
km E of Puerto del Gallo, 8 Aug. 1973 (tl). Johnston el
al. 12125B
at Estacion Mic roondas Las age pan A me 1973 (fl).
Johnston et al. 11457A (TEX); 26 mi.
30. 26 July 1958 (fl). Correll & Toto 20219 (LL
26 (air) mi. SW of Torreon. 6.8 (rd.) mi. NW of Hw . 40
toward Presa Francisco Zarca К Im 6 (fl), Henrick
son & Prigge 15352 (LL). Nue 'vo León: ca. 15 mi.
Matehuela "a IE 57, 24 July 1977 (fl, fr), алм el
MÍ ТЕХ); La Becerra, 5 Sep. 1989 (
ton el s Г (LL); El Barrial, 4 Sep.
17660 (11): La Soledad, 26 Aug. 1940 (fl, fr),
Shreve & Tinkham 9694 (ARIZ); Hacie Ya Pablillo, Gal-
1 t Aug. 1936 (fl). Taylor 172 (AR LL). San Luis

— а
*

—
T

Cand.

Potosí: 6.5 (rd.) mi. S of Arista. in Chihuahuan Desert.
6 Sep. 1971 (fl. fr), Henrickson 6427 (TEX): Ejido Cerrito
Blanco, 10 km al E de Matehuala, 6 Oct. 1980 (fl).
11 (WIS): Charcas, July-Aug. 1934 pil Lundell
(WIS). Tamaulipas: ca. 46 km WNW of Jaumave: 6.5 rd.
km W of Miquihuana. Oct. 1982 (fl). He nrickson 19136b
(TEX): 5 km al N de Estanque de los V km al

Lemus
5517

alles o 25

NW de se beeen ty rife 1986 (f. Hernandez 1917
(TEX). Zacatecas: 5 (rd.) mi. NNE of Rancho Hidalgo.
ca. 27 mi. E ‘amacho, in Chihuahuan Desert

Sep. 1971 (fl. tr ji nrickson 6366b (LL). U.S.A. акне:

‘reek Canyon, Old Wildon Ranch, Big

Bend Nat. ? E Sep. 1966 a), Correll, 33825 (NY):

W side of Old Blue, Glass Mts., 2 June 1941. Warnock
21851 (NY): Big Bend, ee Trail, 7 Mar. 1989 (fl. fr)

Liede & ies m (MO); Chisos Mts
Ише 8115 . Pres di Co.. ca. | mi. is
1941 ^ "aM 2105 (N
of Bats 14 Aug. 1941 (fl. fr),

County not known: Valley of the Rio Ана А
)

3106 (NY).
below Don-
ana. Emory 1057 (I
13. Metastelma schaffneri A. Gray. Proc. Amer.
Acad. Arts 21: 396. 1886. TYPE: Mexico. San
Luis Potosí: near San Luis Potosí. 1876. J. G.
Schaffner 052 (holotype, GH!: (frag-
ment), NY!). Figures 20, 21a-g.

isotype

M i Lge lg S. poy Pr roc. Amer, Acad. Arts
1890. Syn. ne vw Mexico. Jalisco:

mL RN 5 Мах 1888. E . Pringle 1776 (lec-

pe, designated here. NY 002790571: isotypes, К

ч pach, neg. 051460. GH not seen. MI. NYL A

URS

Plants ascending, to 200 cm high: shoots peren-
nial, glabrous, sparsely covered along a single line
with flexuous trichomes; internodes 25-30 em long.
Leaves with petioles 1-2 mm long, with 2 colleters
at blade base; blades 15-25 X 1.5-12
to elliptic to ovate, basally rounded, apically acute

mm, linear
to acuminate, marginally revolute (when dry). adax-
ially sparsely, abaxially isolatedly covered only on
the iris
chomes, 5 um long. Inflorescences 4- to 6-

midrib and the margins with recurved

flowered, 2 to 5 flowers open synchronously, scia-
dioidal, йы; and bracts 0.6-1.2 X 0.3-0.4
glabrous or with tri-

mm at the base. triangular,

chomes on the surface; pedicels 1-3 mm long, gla-

brous. Floral buds 2-2.5 mm long. 1-1.3 mm
diam., ovoid; calyx basally fused. campanulate.

abaxially glabrous or with trichomes, mainly on the
tube: calyx lobes 0.8-1.2 X 0.3-0.5 mm, ovate t
triangular, apically strongly acute: corolla campan-

ulate, 2-3 mm long. abaxially white with purple.
glabrous, adaxially white, smooth trichomes, 150—
180 um long. on the lateral and on the apical parts
of the V^ of total corolla
length, 0.7-0.8 mm wide, patent, ovate, apically
acute; gynostegial corona 0.6-0.8 mm long. longer

lobes; lobes fused to Ca.

than the gynostegium: lobes erect, attached directly

72 Annals of the

Missouri Botanical Garden

7

Uu
8

|

ji

iM

9 2 17

+>

—

—
Ñ

—

0.5mm

Figure 21. Metastelma schaffneri.
n W

a. Habit. —b. Shoot with inflorescences. —c. Flower. —d. Corolla lobe, adaxial
. —e. Gynostegium and corona. —f. Pollinarium. —g. Style-head. a-g. Pringle 1776. Drawn by J. Conrad.

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

underneath the anthers, laminar, ovate. Gynoste-
gium 0.5-0.6 mm high, 1-1.2 mm diam., on a col-
umn 0.3-0.4 mm long; anthers broader than high.
rectangular, abaxially planar; anther wings ca. 400
um long, anther wings of adjacent anthers parallel
to each other, basally widened, in the same plane
as the anther: connective appendages 250—300 jum
long. 350—400 um wide, ovate, narrower than the
stamen, slightly inflexed; pollinarium with corpus-
culum 100—150 jum long, more than twice as long
as broad: caudicles 70—100 um long, cylindrical,
slightly s-shaped, convex-concave; pollinia apically
attached to the caudicles, 150—200 jum long. 80—

100 um wide, ovate in cross section, reniform:
style-head green, 0.8-0.9 mm diam., 0.4—0.5 mm

high. upper part 0.1—0.2 mm high. shorter than the
lower part, depressed-conical. Follicles ca. 55 mm
long, ca. 5 mm diam., obclavate, terete, apically
strongly beaked, medium brown, glabrous: seeds ca.
15 per follicle, 6-6.5 mm long, 3 mm wide. ovate.
sela and aseta side smooth, marginally with ca. 0.5
mm wide wing with entire margin.

Phenology. Collected in flower in June, and
from August to March; in fruit March, August, and
September.

Distribution. Mexico: Baja California, Durango,
Guerrero, Jalisco, Morelos, Nayarit, Oaxaca, Pueb-
la, Sinaloa, Sonora; hillsides and ravines, savanna,
low open deciduous forest; 500-2900 m.

Lectotypification of Metastelma multiflorum is
necessary because there is no clue in the proto-
logue as to where a holotype specimen was depos-
ited. Of the many isotype specimens distributed,
the NY 00279057 specimen is selected because it
is accompanied by a nice drawing.

Of the small-flowered Metastelma species with
dense indumentum on the adaxial side of the co-
rolla lobes. M. schaffneri can be confused with M.
Metastelma schaff-
neri is a species of western central Mexico, while
M. schlechtendalii is distributed along the southern
Gulf Coast, and M. turneri in northeastern Mexico.

schlechtendalii and M. turneri.

Metastelma schlechtendalii is best recognized by its
pollinia, which are ovoid and attached to slightly
geniculate caudicles, while the other two species
have pyriform-reniform pollinia and s-shaped cau-
dicles. Metastelma schaffneri has commonly much
more slender leaves (to 12 mm wide) than M. tur-
neri (to 18 mm wide) and a more slender gynoste-
gium on a longer stipe (0.3—0.4 mm in contrast to
0.1—0.2 mm).

Wiggins 15628, the only specimen from Baja
California, with Metastelma

agrees quite well

schaffneri with respect to leaf indumentum, subses-

sile inflorescences, corona exceeding the shortly
stipitate gynostegium, and geniculate caudicles.
However, corolla indumentum is very short (less
than 100 um), and the corona lobes attach along

the stipe a little distant from the anthers.

Additional specimens examined.
ifornia: Punta San Lorenzo, EUN mi. E of La Paz. 26 Nov.
1959 (fl), li cil 15628 (A urango: Durango &
vicinity. 1896 (fl), үө 159 (NY). Gu

MEXICO. Baja Cal-

rie p near 5
1889 (8), Pringle 2749 (HBG). Mo ЕРИ Ng r-
. 1895 (fl), 5 6205 (НВС. № PU
5). Nayarit: АБ quacatlan, on а S of town, 26 SA p
(fl), Liede & Conrad 2962 (UBT). Oaxaca: 9 km al NE
de Cuicatlán. rumbo а Concepci ión Pápalo, 23 Aug. 1980
. Mendraño 1630 (WIS); Santa Inez Mountains, 15 Oct.
Mes 5626 (ARIZ, LL, NY): above Oaxaca, 7
). Pringle 4766 (НВС, M. NY).
Rancho San qe ‚ 10 a 65 NW de Molcaxac. 15 Oct.
1994 (fl). Tenorio et p: ) (LL); vicinity of due Luis
Tultitlanapa; near wa b 1908 (fl). Purpus 2617
: Tehuacan, lava bed behind El Riego, 4 Aug. 1989
(fl), Linde & edge 2604 (MO). San Luis Potosí: 1879,
ДЙ 313 (Р). Sinaloa:
Feb. 1940 (fl), Gentry 5479 (MO, Кү
oe А 8 Dec. 1939 (fl).
Capadero, Sierra Tacuichamona. 12 Fe 1940 (fl), Gentry
5562 (ARIZ, NY): near roadside at Las Animas beach
near Topolobambo, 28 Jan. 1964 (m. Pes s.n. (LL). So-

T

еу

nora: Сайоп de Bavispe, Aug. 1940 (fl. White 5239
(NY). State unknown: 1905, Purpus 1259 (NY)
14. Metastelma schlechtendalii Decne.. in A. Р.

de Candolle. Prodr. 8: 513. 1844, non Metas-
telma schlechtendalii Chapm., Fl. South. U.S.
366. 1860. nom. Шер. Cynanchum schlechten-
dalii (Decne.) Standl. & Steyerm. „ Publ. Field
Mus. Nat. Hist.. Bot. Ser. : 226. 1947.
TYPE: Mexico. Veracruz: Hacienda de la La-
guna, Aug. 1828, C. J. W. Schiede 159 (lec-
totype, designated by Stevens (2000: 256). P!:
isotypes, HAL not seen, MO not seen, NYL W
not seen).

14а. Metastelma schlechtendalii
schlechtendalii. Figures 22e.

Decne. var.

M puce и Pittier, Contr. U.S. Natl. Herb. 13:

nom. illeg.. non УНЕ 2

die in Cen Symb. Anull. 1: 249. 1899. TYPE:
Ven Оше ‘hé: San O т. А ы:

T. Heyde & E. Lux 5060 n

S not seen; isotypes, F о seen, M!, NY!. UPS).

Metastelma parv ani 5с ehh. nnaea 6: 731. 1831.

m. illeg.. non 1 ar R. Br. ex

Schult., in Roemer & Schultes, Syst. Veg. 6: 120.

1820. TYPE: Mexico. Veracruz: Hacienda de la La-

guna, Sep. 1828, Schiede 260 (holotype. НАШ; iso-

type, HAL!).

Plants ascending, 80-150 em high: shoots an-

Annals of the
Missouri Botanical Garden

Figure 22. Metastelma schlechtendalii.

enicola, e: M. schlechtendalii var.
Gynoste spo and corona.
J. Conrac

ore view. —d, d"
ЗІ.

: Molina 15672.

Drawn

by

schlechte ote —
€

a

VUE

ENS

padal anm
7

А

CS
* DANN

Jy

7 4)
E,

Tow

: M. schlechtendalti var. trichophyllum. d M. йн dice var. ar-
a’. Shoot with inflorescences. —b'. Flower. —c'. Corolla lobe,
e”. la —{'. $ lb a NA Molina m d“: Gentry

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

rB

o
SA м | | : |
m xp M | $ | q
3 " Е \ € |M
ni 0 2 \ f ff A Dy
a М \ / 1b |
EE «NS OE S Tr | as
. 3 \ р аі
i N Ph f. } А gore
X Plus r (oun
| \, i g e a
) ps Pà l A.N ө | Ы
ES ^ u а En \ f. e e e
_ — — y ADAN = 6 EM е, a 20°
ZA | LN Я
SS Y Г = е at |
— Ф. | nm
SI — < |
| à ? Ps „^^“ = к e “a
| — - oan 5 KR 15°
} A. ^a +
Кы 3
me р x
= — — + о Уй ло
ө M. schlechtendalii var. schlechtendalii | у
4 M. schlechtendalii var. arenicola kg
А M.schlechtendalii var. trichophyllum |
| — | - 5?

-110* -105* -100*

Distribution of Metastelma schlechtendaliü.

-115°

Figure 23.

nual, glabrous, sparsely to densely covered along a
single line with recurved to flexuous trichomes.
150—300 um long: internodes 2-5 cm long. 0.5-1
mm diam. Leaves with petioles 1-5(-10) mm long.
with O to 2 colleters at blade base: blades 15-15

X 4-15 mm, elliptic to ovate, basally cuneate to
rounded, apically acute to acuminate, adaxially gla-
brous or isolatedly to sparsely covered only on
veins and margins (except for Aguilar 124 with iso-
lated trichomes on the lamina). with appressed tri-
chomes, ca. 200 pm long. abaxially glabrous or
on veins and mar-
gins with appressed trichomes, 200-300 um long.
Inflorescences 2- to 12-flowered, all flowers open
synchronously, sciadioidal, bostrychoid: peduncles
(2-)4-15 mm long, glabrous, isolatedly to sparsely

very isolatedly covered mainly

covered along a single line with recurved tri-
chomes, 200—300 рт long. Flowers very sweetly
fragrant; floral bracts 0.5—0.7 X 0.2-0.3 mm at the
base, ovate, glabrous or ciliate; pedicels 1.5-2.5 mm
long. glabrous, isolatedly to sparsely covered along
a single line with recurved trichomes, 100—150 ¡um

long. Floral buds ca. 2.5 mm long, ca. 1 mm diam.

ovoid: calyx basally fused, campanulate. abaxially
with a few sparse trichomes mainly on the tube:
calyx lobes ca. 1 X ca. 0.4 mm, ovate, apically
acute: corolla campanulate, 2-3 mm long. abaxially
white. glabrous, adaxially white, with verrucose tri-
chomes, 150-200 um long, on the apical and on
the lateral parts of the lobes: lobes basally fused.
0.6—0.7 mm wide, erect to patent, ovate to lance-
olate. apically acute: gynostegial corona 0.8—1 mm
long. slightly longer than the gynostegium: lobes
erect, attached along the stipe. laminar, triangular.
Gynostegium ca. 0.5 mm high, ca. | mm diam.. on
a stipe 0.6-0.8 mm long: anthers broader than high.
rectangular. abaxially planar: anther wings 150—
200 um long. extending along the entire length of
the anther, anther wings of adjacent anthers par-
allel to each other, in the same plane as the anther:
connective appendages ca. 200 um long. ca. 150
um wide, ovate, narrower than the stamen. strongly
inflexed: pollinarium with corpusculum. 120-150
um long. between 1.5 times and twice as long as
broad, ovoid; caudicles 100-130 um long. evlin-

drical, slightly geniculate; pollinia apically at-

Annals of the
Missouri Botanical Garden

tached to the caudicles, 150-180 um long, 80—100
um wide, ovate in cross section, clavate; style-head
white, 0.5-0.6 mm diam., ca. 0.25 mm high, upper
part 0—0.1 mm high, shorter than the lower part,
flat to umbonate. Follicles one per flower, 35—40
mm long, 2-3 mm diam., fusiform, terete, apically
strongly beaked, dark brown, glabrous; seeds ca. 5.5
mm long, ca. 3 mm wide, oblong, light brown, seta
side tuberculate, aseta side smooth, marginally with
0.5 mm wide wing with irregularly denticulate mar-
gin; coma ca. 20 mm long.

Phenology. Collected in flower from July to
April; in fruit in November.

Distribution. Belize: Corazal, Orange Walk, To-
ledo; Guatemala: Guatemala, Jutiapa, Quetzalten-
ango, Quiché; Honduras: Colón, Ocotepeque; Mex-
ico: Campeche, Quintana Roo, Veracruz, Yucatán;
very wide ecological amplitude, sand dunes, salt
marshes, roadside vegetation, thickets, disturbed
forests; sea level to 2000 m.

Literature and illustrations. Pitter (1910: fig.
4а, b).
Williams (1968) included Metastelma decipiens
Pittier in the synonymy of M. schlechtendalii var.
schlechtendalii because they share narrowly oblong-
lanceolate corolla lobes that are adaxially densely
barbellate, a corona attached along the stipe and
slightly exceeding the gynostegium, and lanceolate
or ovate-lanceolate leaves with trichomes only on
veins and margins

Metastelma sc hes htendalii var. schlechtendalii is
a frequent species especially in lowland areas
around the Yucatán Peninsula and up to 2000 m
in Guatemala and Honduras. In the Yucatán, it is
often difficult to distinguish from short-stiped, only

vaguely barbate specimens of M. barbigerum var.

liesnerianum, but the transversely oblong outline of
the gynostegium is diagnostic against the conical
gynostegium of the M. barbigerum complex. How-
ever, there seems to be a lot of hybridization and
introgression between the two species complexes
especially in the Yucatán, judging from the numer-
ous specimens with somewhat intermediate char-
acters.

Metastelma schlechtendalii var. schlechtendalii is
easily confused with M. schaffneri and M. turneri,
but can be distinguished by its conspicuously pro-
truding anther wings (short and almost vertical in
the other two species), and its flat-topped gynoste-
gium with strongly inflexed anther appendages
(rounded to slightly conical gynostegium with
slightly inflexed anther appendages in the other two
species

Metastelma | schlechtendalii var.

schlechtendalii

has often been confused with M. parviflorum R. Br.
ex Schult., a widespread taxon in northern South
America and the Caribbean, but it is clearly distin-
guishable by its only basally fused corolla and the
corona lobes attached along the stipe, and not, as
in М. parviflorum, at the base of the stipe, fused to
Schlechtendal (1831: 731)
commited exactly this error in his brief enumera-
tion. Two years later (Schlechtendal, 1833: 518), he
indicated the specimen on which he based his con-
clusion, Schiede 260, collected at the same locality
as the lectotype of M. schlechtendalii, Schiede 159.
Decaisne (1844) noted the error, and TROPICOS

takes the same view.

the corolla. However,

T specimens examined. BELIZE. Corazal:
ca. 4 km SE of Sarteneja, 18 Mar. 1987 (f ч Dile ho
Brant 32667 L, . Orange Walk: Honey Camp,
Oct. 1929 (fl), Lundell 651 (NY). Toledo: Monkey ho
Swansea branch, 26 Nov. 1941 (fl), Gentle 3815 (LL, NY).
GUATEMALA. Guatemala: along Hwy. 18 about 7.2 mi.
E of San José Pifiula, 16 July 1971 (fl), Stevens 1250 (NY,
TEX). Jutiapa: Д 178 de а Арг. 1894 (fl),
Heyde & Lux 63: : La Libertad, 2 June
1933, Lundell Pp (W IS); eee Road. km 82, 21 Nov.
196 , Contreras 7237 (LL); Santa Ana, 20 km al E de
See Elena, 13 Nov. 1965 (fl), Molina 15672 (NY); al-
rededor de Libertad, 30 km de Santa Elena, 22 ds 1970
(fl), Тип Ortiz 604 (NY); Santa Elena, en el camino para
Santa Marta, a km 3, lado N, 12 Dec. 1970 (fl), Tún 0
1494 (NY); San Miguel, Savanna San Miguel, 3 km Мо
San Miguel, 8 Dec. 1967 (fl), Contreras 7270 (LL); na
Nat. Park, Bajo de Santa Fé, salida de Arroyo Corriental,
17 Jan. 1964 (fl), Contreras 3866 (LL). 5
Palmar, 13 Oct. 1934 (fl), Skutch 1438 (NY). District not
known: St. Tomas, 1841, Friedrichsthal s.n. (NY). HO
DURAS. Colón: 1.8 mi. strip on N bank of Río Guai-
moreto, NE of Trujillo on old rd. to Castilla, 11 Dec. 1980
(fl), Saunders 740 . Ocotepeque: El Cerro, vi-
San Шиш; 30 ae 1968 (i). Molina 22442
(NY); 9 Lempa river, rd. to Esquipulas, 29 Aug. 1968
(fl), Molina 22438 (NY). MEXICO. Campeche: alrede-
dores de las grutas de Xtac arie a 3 km al O de
Bolonchen de Hejón, 29 Sep. 1985 (fl), Cabrera & De
e а NY); Zona "iiu. ч de Campeche, 28
Oct. 7 (fl), Gutiérrez 5462 (TEX). Quintana Roo: en
la a ión a Laguna Ocum, a E km al Sur de GF.
Carrillo Puerto, 13 Nov. 1980 (fl), Cabrera & Cortez 261
NY); Punta Bete, donde
Jan. 1980 (fl), Sousa et al. Я
Alto Lucero, Boca / 5 о 1971 (fl), Dorantes 385
T a Hacie de la со Schiede 11 (HAL); Хега-
‚ Wawra 625 (NY); Zac ‘марап and vicinity, Nov. 1906
(A), 7 ?urpus por (NY). Yucatán: 30 mi. E of Mérida at
Hoctun, 7 Mar. 1973 (fl), Butterwick 78 (TEX); Uayma,
ca. 20 km NW von Valladolid, 21 Nov. 1981 (fl, fr). oon
& Geiseler 7016 (B), Feb. 1916 (fl), Gaumer 23436 f
Progreso, E of port, ч 1938 (fl), Lundell & may 8113
TEX); along dirt rd. to Chamul SW of village, 14 Oc
1989 (fl), Mogensen 1151 (NY). State un. Berlandier
$

s.n. (

p
—
—

pm
E
—

ж,

Volume 91, Number 1

Liede & Meve 77
Revision of Metastelma

Decne. var.
TYPE:
Mexico. Sonora: Mesa Masiaca, just N of the
microwave tower, 6.5 km (by air) WNW of San
José de Masiaca, ca. 200 m, 22 Nov. 1993, y
W. 1 93-358 (with C. D. Bertelsen,

A. Meyer, K. J. Johnson, M. M. Steinmann, A
R. van Bere & F Wiens) (holotype.
ARIZ!). Figures 22d", 23.

14b. Metastelma schlechtendalii

arenicola Liede & Meve, var. nov.

arietas varietati schlechtendalii similis, sed dif-
fert d sn entibus subsessilibus, bracteis sepalibusque
lanceolatis, corona staminali gynostegium multo super-
anle.

Plants ascending: shoots perennial, basally
woody, with gravish brown bark. sparsely covered
along a single line or over the entire surface (Gentry
5431) with erect or recurved trichomes, 200—250
um long: internodes 2—4 em long, 0.5-1 mm diam.
Leaves with petioles 2-5 mm long. with 0 to 2 col-
leters at blade base: blades 5—25(—50) X 4-10 mm,
ovate to linear, basally rounded to cuneate, apically
acute to acuminate, adaxially isolatedly to sparsely
covered only on the midrib and margins with re-
curved trichomes. 150-200 um long, abaxially gla-
brous. Inflorescences always one per node, extra-
2 to 7
subsessile, rarely pe-

axillary, 3- to 8-flowered, flowers open

synchronously, sciadioidal,
dunculate with peduncles to 4 mm long, densely
covered along a single line with recurved tri-
chomes. 150-200 um long; floral bracts 0.7-1 X
0.2-0.3 mm at the base. lanceolate, glabrous; ped-
icels 1.5-3 mm long, sparsely to densely covered
along a single line with recurved trichomes, 100-
150 um long, rarely glabrous. Floral buds ca. 2.5
mm long, ca. 1.2 mm diam.; calyx basally fused,
campanulate, abaxially with a few sparse trichomes,
calyx lobes 0.8-1.3 X 0.30.5

lanceolate, apically acute; corolla campanu-

mainly on the tube;

abaxially white, glabrous,
100—150
wm long. on the apical and on the lateral parts of
the lobes: lobes basally fused, 0.5-0.7 mm wide,
erect to patent, ovate, apically acute: gynostegial

2.5-3 mm long.

adaxially white, with smooth trichomes.

corona 1.2-1.5 mm long, distinctly longer than the
gynostegium; lobes erect to inflexed, attached along
the stipe. laminar, triangular. Gynostegium 0.7—

mm high, 0.3-0.4 mm diam., on a stipe 0.5-0.6
mm long: anthers broader than high, rectangular,
abaxially planar; anther wings 200—250 jum long,
extending along the entire length of the anther, an-
ther wings of adjacent anthers parallel to each oth-
er; connective appendages ca. 500 um long. ca.
300 um wide, ovate, narrower than the stamen,
slightly to strongly inflexed: pollinarium with cor-

pusculum ca. 150 jum long, between 1.5 times and
twice as long as broad, ovoid; caudicles ca. 80 um
long. cylindrical, slightly geniculate; pollinia api-
cally attached to the caudicles, ca.
ca. 80 um wide, ovate in cross section, ovoid: style-
0.4-0.5 mm high.
upper part ca. 0.2 mm high. equaling the lower

Um long.

head white, ca. 0.7 mm diam.
part, distinctly umbonate or flat (Gentry 5431). Fol-
35-45 mm long, 4—5
obclavate, terete, apically shortly beaked,

licles one per flower, mm
diam.,
dark brown to black, glabrous; seeds 5-6 mm long.
3—4 mm wide, ovate. medium brown, seta and aseta
side tuberculate, papillose with regularly arranged
papillae, marginally wingless, denticulate: coma
20-30 mm long, yellowish.

Phenology. Collected in flower in January, and
from September to November: in fruit in October.
Distribution. | Mexico: Sinaloa, Sonora: littoral

sand hills, basaltic slopes, thornscrub and thorn
forest; 30—400 m.

In addition to the diagnostic characters of the new
variety (subsessile inflorescences, lanceolate bracts
and calyx lobes, and a corona considerably exceed-
ing the gynostegium),
(70%) have a slightly elevated style-head. while the
style-head is flat to slightly umbonate in the other

the majority of specimens

two varieties throughout. The variety is restricted to
the western Mexican lowlands, separated by at least
1000 km from the other two varieties.

Gentry 5431 does not fit the description of Me-
tastelma schlechtendalii var. arenicola perfectly: its
shoots are sparsely, but evenly, covered with tri-
chomes (in all other specimens, the trichomes only
occur along a single, though occasionally rather
broad, line), floral bracts and sepals are compara-
tively short, the flowers relatively large, and the
style-head is flat. Nevertheless. gynostegium shape
and the protruding anther wings make it a member
of the M. schlechtendalii complex and it is best ac-

commodated here.

Paratypes. MEXICO. Sinaloa: Altata, 31 Jan. 1940
(fl), Gentry 5431 (ARIZ, | pues abampo. 10 Oct. 1962
(fl), Skorepa 173 (WIS): nr. Yacht Hotel, e 5
Oct. 1964 (fr). Turner & Hastings 64-128 (ARIAL
ra: summit of Cerro Prieto, vic. of microwave station, 15
km E of Navojoa above rd. 1 5 Sep. 1989 (fl).
Sanders 9265 (ARIZ): Mesa Masiaca y vic inity, at summit
of M.M. microwave tower, 6.5 km (by E of San Jose
de Masiaca, 23 Sep. 1994 (fl), Friedman 379- 94 (ARIZ).

Sono-

14е. Metastelma schlechtendalii Decne. var.
Williams)

Basionym:

trichophyllum (L. Liede &
Meve,
chum trichophyllum L. O. Williams, Fieldiana.

Bot. 32: 41. 1968. Metastelma trichophyllum

comb. et stat. nov. Cynan-

78

Annals of the
Missouri Botanical Garden

(L. О. Williams) W. D. Stevens, Phytologia 64:
335. 1988. TYPE:
› Telica, camino de Montaña Uval, 20
1903. A. Molina R. 13344 (holotype, Fl;
isotypes, EAP not seen, NY! TEX!) Figures
22a'-f', 23.

Honduras. Olancho: Cerca

Plants ascending, to 500 cm high; shoots peren-
bark,

densely covered over the entire surface or along a

nial, basally woody, with grayish brown
single line with erect trichomes, 300—400 um long;
internodes 2-5 cm long, | mm diam. Leaves with
petioles 2—5 mm long, with 2 colleters at blade
base; blades 15-35 7-15 mm, ovate, basally
rounded, apically acute to acuminate, adaxially and
abaxially sparsely covered over the entire surface
with erect trichomes, 250—300 um long. /nflores-
cences always one per node, (4—)6- to 12-flowered,
4 to 8 flowers open synchronously, sciadioidal: pe-
duncles 5-15 mm long, densely covered over the
entire surface or along a single line with erect to
recurved trichomes, 300-400 um long; floral bracts
0.35-0.4 х 0.2-0.3 mm at the base, ovate, ciliate:
pedicels 3-5 mm long, sparsely to densely covered
over the entire surface with erect trichomes, 300—
400 um long. Floral buds 2-2.3 mm long, 1-1.2
mm diam., ovoid; calyx basally fused, campanulate;
calyx lobes ca. 0.8 X ca. 0.3 mm, ovate, apically
acute: corolla cyathiform to campanulate, 2.5—3(—
4) mm long. abaxially cream to yellow. glabrous,
to 200

um long, on the apical and on the lateral parts of

adaxially white, with verrucose trichomes,

the lobes: lobes basally fused, 0.5-0.7 mm wide,
patent, ovate, apically acute; gynostegial corona
0.8-1 mm long, equaling to longer than the gynos-
tegium; lobes erect, attached along the upper third
of the stipe, lanceolate, extended into a filiform tip.
Gynostegium ca. О.А mm high, 0.8—1 mm diam., on
a stipe 0.6-1 mm long: anthers broader than high,
rectangular, abaxially planar: anther wings 200—
300 um long, extending along the entire length of
the anther, anther wings of adjacent anthers par-
allel to each other, in the same plane as the anther;
connective appendages ca. 250 um long. ca. 150
um wide, ovate, narrower than the stamen, strongly
inflexed; pollinarium with corpusculum. 120-150
um long, between 1.5 times and twice as long as
broad, ovoid; caudicles 100-120 um long, cylin-
pollinia apically at-
180-200 um long, 80-100
um wide, ovate in cross section, clavate; style-head

drical, slightly geniculate;

tached to the caudicles,
white, 0.5-0.6 mm diam., ca. 0.25 mm high, upper
part flat. Follicles (fide protologue) 25-50 mm long,

4-5 mm diam., obclavate, terete, apically strongly

beaked, wingless, with dense indumentum: seeds
not seen.

Phenology. Collected in flower from August to
November.

Distribution. El Salvador; Honduras: Morazán,
Olancho; Mexico: Chiapas; matorral, secondary

vegetation, tropical deciduous forest; (500—)800—
2100 m

en schlechtendalii var. trichophyllum is
easily separated from the typical variety by the
dense, equally distributed indumentum on stems
and leaves. In addition, inflorescences appear to
bear more flowers in variety trichophyllum, a char-
acter hard to judge from herbarium specimens, as
they might not have been picked at the peak of
flowering. The distribution area of variety tricho-
phyllum is disjunct between Chiapas (Mexico) and
Honduras-El Salvador, with a gap in Guatemala,
where the typical variety colonizes even the higher
elevations. In Honduras, the typical variety and va-
riety trichophyllum both occur, but variety tricho-
phyllum seems to prefer higher altitudes there.
However, as the floral characters fully agree with
those of the M. schlechtendalii complex and the dis-
tribution areas of the typical variety and variety
trichophyllum are continuous to somewhat overlap-
ping in Honduras, varietal (rather than specific or
subspecific) rank for the taxon is appropriate, even
though it is one of the easiest Metastelma taxa to
recognize in the field by virtue of the equally dis-
tributed indumentum on the leaves.

ано specime ns examined. EL SALVADOR. San
Salvador, 1271 (NY). HONDURAS. Mor-

azan: е ЕИ ELC par Cerro de Hule 20 km

Calderón

' of ا‎ 27 Oct. › (fl), Molina 18455 (NY):
Ojojona, 45 km S de Терис al 28 a 1985 (fh). Aspra
65 (В); near Rio Guac pug & Los Laureles, NW of Te-

gucigalpa, 4 Nov. 1966 (fl). inei ub (NY). Olan-
cho: Carretera у pu del Río Juticalpa, 6 km de Ju-
ticalpa, 18 Nov. 1963, Molina 13226 (NY. TEX): Valle
Le rp entre El Zarzal y empalme a Galeras, i oS
ч 3 (fl) Molina 13370 (NY). MEXICO. Chia rd.
1967 (ch. Ton 3092

from kl Bosque to Simojovel, 10 Oct.
TEX); near microwave station of La Mina, 12 km S of
X 190 nr Rizo de Oro. 16 Oct. 1971 e» Breedlove &

Thorne 20658 (TEX); a 22 km al N de Ocozoc Pepe cam-
mo a 0 24 Oct. 1985 (fl), Martinez 1428 (LL); 10
m SW of Ocosingo along rd. to San С deny 23 Sep.
1972 (fl), hu; оде 27820 (NY, ТЕХ); Puebla Nueva, 21
Oct. 1987 (fl), Pérez 85 (NY, TEX): Colonia Choro, 15 85
1966 io Ton 1548 (Т EX); La Roblada, Ocozocoautla, 15

Nov. 1971 (f. MacDougal H116 (NY); Las Rosas on rd.
to ee ‘nustiano Carranza Aug. 1965 (fl). Roc et al. 997
(paratype, NY, WIS); 15 km SW of Suchiapa along rd. to

Villa Flores, 3 Oct. 1972 (fl), Bree diu 26258 (NY, TEX).

15. Metastelma stenomeres (Standl.
erm.) W. D. Stevens, Phytologia 64: 335.

—

& Stey-
1988.

Volume 91, Number 1

Liede & Meve
Revision of Metastelma

—
—

Id
>

ME
OS

RATA,

pt
Vere ds

55
. Ee
hate RA

=

Figure

24.

d. Gynostegium and corona. —e.

Metastelma stenomeres.

a. Shoot Vis е
-head. a-f: Schipp 674

Pollinarium. —f.

. Flowe

orolla lobe.

pq =f

. Drawn b J. Conra

adaxial view.

Annals of the
Missouri Botanical Garden

stenomeres Standl. & Steyerm.,
Publ. Field Mus. Nat. Hist., Bot. Ser. 23: 224.
1947. TYPE: Belize. All Pines, 2 m, 5 Feb.
1930, W. A. Schipp 674 (holotype, F not seen:
isotype, NY). Figures 12, 24a—

Cynanchum

Plants ascending, 50-150 cm high: shoots pe-
rennial, glabrous; internodes 4—6 cm long, ca
mm diam. Leaves with petioles 4-6 mm long, with
0 or l colleter at blade base; blades 25-50 x 5-9
mm, slenderly elliptic or lanceolate, basally acute
to cuneate, apically acute to acuminate, adaxially
and abaxially glabrous. /nflorescences occasionally
two per node, extra-axillary, 8- to 12-flowered, all
flowers open synchronously, sciadioidal, but some-
times basally dichasial; peduncles 3—5 mm long,
sparsely to densely covered along a single line with
recurved trichomes, 100-200 um long. Flowers
sweetly fragrant; floral bracts 0.4—0.6 X 0.2-0.3
mm at the base, ovate, glabrous; pedicels 3-5 mm
long. glabrous. Floral buds 3.5—4 mm long, 1.2-1.5
mm diam., slender ovoid; calyx basally fused to
fused for ca. % of its length.
very sparsely covered with trichomes; calyx lobes
0.6—0.8 х 0.2-0.4 mm, ovate, apically acute to ob-
tuse; corolla salverform, 4—4.5 mm long, abaxially
white, glabrous, adaxially white, adaxially with ver-
rucose trichomes, to 300 um long, on the lateral
parts of the lobes; lobes fused for ca. Y of total
corolla length, 0.8-1
slenderly ovate, apically obtuse: gynostegial corona
than the gvnostegium; lobes

campanulate, abaxially

mm wide, erect to patent,
2 mm long. longer
erect, attached. directly
laminar to filiform, lanceolate, extended into a long,
slender tip. Gynostegium ca. 1.3 mm high, 0.7 mm
without appendage of style-head, ca. 0.8 mm diam.,

underneath the anthers,

on a column ca. 1.3 mm long; anthers broader than
high, rectangular, abaxially planar; anther wings
0.3 um long, extending along the entire length of
the anther, in the same plane as the anther; con-
nective appendages 150 um long, 300 um wide.
ovate, narrower than the stamen, strongly inflexed:
pollinarium with corpusculum ca. 150 um long, be-
tween 1.5 times and twice as long as broad, ovoid;
caudicles ca. 150 um long, cylindrical, geniculate:
pollinia apically attached to the caudicles, ca. 200
um long. са. 100 um wide, elliptical in cross sec-
ca. 0.4 mm diam.,
ca. 0.6 mm high, 0.4 mm high.
equaling or longer than the lower part, obinfundi-
buliform or conical. Follicles one per flower, ca. 5X

tion, pyriform; style-head white,

upper part ca.

=

mm long. 4 mm diam., obclavate, terete, apically
strongly beaked, light gray-brown, wingless, gla-

brous; seeds unknown.

Phenology. Collected in flower in February and
from August to October.
Distribution. Belize; in open pine forests, ham-

mock edges; lowlands.

A well-distinguished species endemic to Belize,
which is most easily recognized by its floriferous
inflorescences, the slender outline of the flowers,
the very long (to 2 mm), acute and membraneous
corona lobes, the long (to 1.3 mm) and slender col-
umn carrying corona and gynostegium, and the usu-
ally pronounced central elongation (to 0.4 mm) of

the style-head.

Additional specimens examined. BELIZE. Broken
1 8 mi. NE of Boomtown, 17 Sep. 1936, O'Neill 8660
(NY. WIS); near Manatee, 15 ч 1940 (fl), Gentle pad
(NY, TEX); Monkey River, nr. Jenkins Creek,

1942 (fl), Саш 4190 (NY, TEX): Mountain Pi e > Ride,
San к July-Aug.. 1936 (Н), Lundell 6656 (NY,
TEX, ; Mullins River rd., 15 Nov. 1954 750 Gentle
8458 TEN. Traci i des k, Sibun River, 10 Aug. 1935 (fl),

IS).

TC

un 1755 (NY,

16. Metastelma turneri Liede & Meve, nom. et

stat. nov. Basionym: Cynanchum | maccartii
Shinners var. latifolium Turner ex Henrickson,
Sida 12: 98. 1987, non Metastelma latifolium
Hose, Contr. U.S. Natl. Herb. 1: 106. 1891
TYPE: Mexico. Nuevo León: Las Anacuas,
Mpio. Linares, 640 m, 5 Aug. 1980, С. S. Hin-
ton 17935 (holotype, TEX not seen). Figures
15, 25a-f.

Plants ascending, 150-200 cm high: shoots pe-
rennial, basally slightly woody, with greenish to yel-
lowish brown bark, sparsely covered along a single
line with recurved trichomes, 200—350 um long:
internodes 2—5 cm long, ca. 1 mm diam. Leaves
with petioles 2-10 mm long, with 1 or 2 colleters
at blade base; blades 10—40(—50) х 5-18 mm,
ovate to lanceolate, basally rounded, apically acu-
minate, marginally revolute (when dry), adaxially
isolatedly to sparsely covered, mainly or only on
the midrib and margins with recurved trichomes,
150-250 um long, abaxially glabrous or with a few
recurved trichomes on the midvein. /nflorescences
always one per node, extra-axillary, 3- to 8-flow-
ered, 2 or 3 flowers open synchronously, sciadioi-
dal, subsessile; floral bracts 0.4—0.7 X 0.2-0.3 mm
at the base, lanceolate, ciliate; pedicels 2-4 mm
long, covered along a single line with recurved tri-
chomes, 200-250 jum long. Floral buds ca. З mm
long, ca. 1.5 mm diam., ovoid; calyx basally fused,
campanulate, abaxially glabrous or slightly verru-
cose, ciliate; calyx lobes 0.5-1 X 0.3-0.5 mm,
ovate, apically rounded: corolla subcampanulate,
2.54.0 mm long, abaxially creamish white, gla-

Volume 91, Number 1
2004

Liede & Meve 81
Revision of Metastelma

, 025mm ,
' 05mm

Figure 25. Metastelma turneri. —a. Sho
Gynostegium with corona. —e ‚ Pollinartuin: f. Style-he

brous, adaxially creamish white, with smooth tri-

chomes, 50-200 um long. on the apical and on the

than lateral ones, and scattered deflexed hispid tri-
chomes on the central parts of the lobes; lobes ba-
| i ovate to lan-

sally fused, 0.7-1 mm wide, patent.

d

ot with inflorescences. —b. Flower. —c.

ad. a: Hinon 17776. b-f: 7 75 11841.

ateral parts of the lobes, apical trichomes longer

rolla lobe. adaxial view. —d.

Drawn by U. Meve.

ceolate, apically acute; gynostegial corona 0.7-1
mm high, equaling to longer than the gynostegium:
lobes erect, apically slightly reflexed, attached di-
rectly underneath the anthers, laminar, ovate. Gy-
legume 0.6-1 mm high. 0.5-0.8 mm diam.. on

a stipe 0.1-0.2 mm long: anthers longer than broad.

82

Annals of the
Missouri Botanical Garden

trapezoidal, abaxially rounded; anther wings 200—
250 um long, not extending along the entire length
of the anther; anther wings of adjacent anthers par-
allel to each other, slightly centrifugal; connective
appendages 200—250 um long, 250—300 um wide,
ovate, narrower than the stamen, slightly inflexed:
pollinarium with corpusculum. 100—150. um long.
between 1.5 times and twice as long as broad, el-
прис; caudicles ca. 100 um long, cylindrical,
strongly s-shaped, convex-concave; pollinia apical-
ly attached to the caudicles, 130—220 jum long, ca.
100 um wide, ovate in cross section, pyriform:
0.2—0.3 mm
high, upper part ca. 0.1 mm high, shorter than the
lower part, flat to umbonate. Follicles 45-55 mm

style-head white, 0.5-0.7 mm diam.,

long. 5-6 mm diam., terete, apically strongly
beaked, dark brown, glabrous; seeds 6—7.5 mm

long, 3—4 mm wide, ovate, dark brown, seta and
aseta side smooth, marginally with 0.5-0.7 mm
wide wing with slightly irregular margin; coma ca.
20 mm long.
Phenology. Collected in flower in May, July.
August, and October; in fruit in October.
Distribution. Mexico: San Luis
Potosí, Tamaulipas; on dry hillslopes in scrub; 400—

nm.

Nuevo León,

Literature and illustrations. Henrickson (1987:
98, fig. 1)

Henrickson (1987) considered Metastelma tur-
nert a variety of M. palmert, with which it shares
the general shape of the corona. However, not only
are the leaves and the flowers of M. turneri usually
larger than those of M. palmeri (leaves: 16-35 X
2.5-7 mm vs. 10-40(-50) X 5-18 mm, ine up
to 4 mm vs. up to 3 mm, respectively), but also the
indument of the adaxial side of the corolla lobes in
M. turneri is more reminiscent of M. schlechtendalii
than of M. palmeri with the apical trichomes con-

spicuously longer than the lateral ones.

A new name has to be chosen for this species
because Metastelma latifolium Rose (1891) has pri-
orit y.

One specimen (Mexico. bise rd. to Bus-
tamente N of La Presita & 2.7 mi. N of Hwy. 70,
21 May 1982 (fl), Dorr 2359, TEX) shows the co-
rolla lobe indumentum of Metastelma turneri, but
the leaf shape and flower size of M. palmeri and is
assumed to be a hybrid between the two species.

Additional specimens 5 MEXICO. Nuevo

León: К! Chipinque. ca. 6 km al sur de
ino а la е 7 Oct

Monterrey, cam-
. 1998 (fl. fr). lane al & Carranza

s.n. (TEX); Linares, 12 May 1980 (fl), Rzedowski 17776
ТЕХ); ера jos А Monterrey, 17 Aug. 1903 (fl).

Pringle 11841 (TEX); Montemorelos, 10 Aug. 1988 (f).
Patterson 6476 m Villa Santiago, Cañon de Potrero

ои A July — (fl). scd 2099 (NY, TEX). ye
is Potosí: 75 km N of S uis Potosí, on side rd. t
mal 'ázar at km 11 . 19 July 1982 (fl), Fryxell 3820
). Tamaulipas: Tm km NW of Palmillas on P to ahs
1 8 14 Aug. 1941 (fl), Stanford et al. 920 (N
2341); Mpio. Victoria, Altas Cumbres, 29 June е i
3 1534 (TEX).

EXCLUDED NAMES

Metastelma angustifolium Turez., Bull. Soc. Imp.
vaturalistes Moscou. 1852(2): 315. 1852.
TYPE: Mexico. Miradores, alt. 3000 ped.", J.

Linden 1353 (holotype, P!).

A member of the genus Orthosia.

Metastelma eulaxiflorum (Lundell) Liede, Novon 7:
41. 1997
Wrightia 5:

¿ynanc hum ا‎ Lundell,
351. Jobinia eulaxiflora
(Lundell) W. D. e Novon: 244, 2000
TYPE: Guatemala. Baja Verapaz: Union Bar-
rios, high forest hilltop, E of km 154, 8 June
1975, C. L. Lundell & E. Contreras 19401 (ho-
lotype, LL!; isotypes, MO not seen, S!

Transferred to the previously exclusively South

American genus Jobinia E. Fourn. by Stevens
(2000) because of its paired, axillary. diffusely pa-

niculate inflorescences.

Metastelma 5 Standl., Publ. Field Mus.
Nat. Hist., Bot. Ser. 18: 956. 1938. Cynan-
chum pe (Standl.) L. O. Williams,
Fieldiana, Bot. 32: 36. 1968. TYPE:
Rica. Entre San Ramón y La Palma de San
Ramón, June 1928, A. M. Brenes 6179 (holo-
type, F not seen: isotype, NY!).

Costa

This species is the only presently known member
of the genus Scyphostelma Baill. (formerly *Cynan-
chum" sect. Microphyllum) in Central America be-
cause of its basally fused corona and its character-
istic branching pattern of long shoots and short
shoots bearing distichously arranged leaves.
Metastelma glaberrimum Woodson, Ann. Missouri
Bot. 107: 17. 1937. Cynanchum glaber-
rimum (Woodson) L. O. Williams,
Bot. 32: 36. 1968. TYPE:
valley of the upper id Chiriquí А пеаг
Monte Lirio, ca. 1830 m, 11 July 19
Seibert 300 кен 0. bas. 5 по!

seen).

Gard.
Fieldiana,
Panama. Chiriquí:

A member of the genus Orthosia because of its
basally fused corona and adaxially glabrous corolla
lobes.

Volume 91, Number 1
2004

Liede & Meve
Revision of Metastelma

. Williams) W. D. Ste-
1988. C ynanchum
miserum ^r О. Williams. Fieldiana. i
38. 1968. TYPE: Guatemala. Alta Verapaz: Im
да in i Pansamala, alt. 1260 m. July 1887,
Н. v. Tuerckheim 1290 (holotype, US!; isotypes.
P^.

Metastelma miserum (l. €

vens, ra "M

F not seen, GH not seen,

A member of the genus Orthosta because of its
basally fused corona and adaxially glabrous corolla
lobes.

Metastelma pubescens (Greenm.) W. D. Stevens.
405. 1983. Astephanus pubes-
Acad. Arts 32: 209
Morelos: wet bar-
above Cuernavaca, 2100 m. 21 Sep.
C. C. Pringle 6507 (Fl, GH! P! MO not
NYD: "in the mountains near Cuerna-

” 3 Aug. 1896, C. C. Pringle 7203 (GH!).

Phytologia 53:
cens Greenm.. Proc. Amer.
1897. SYNTYPES: Mexico.
ranca
1896.

seen,

—

vaca.
A member of the genus Orthosia because of its
adaxially papillate (but not. indumented) corolla
lobes. green stems. double inflorescences, and twin
follicles.
Metastelma rubens (L. O. Williams) W. D. Stevens.
Phytologia 64: 335. 1988. каш = rubens
L. O. Williams. Fieldiana. Bot. . 1968.
TYPE: Guatemala. a ia Santa
Elena. 2400-2700 m, 27 July 1933, A. К
Skutch 503 (holotype, US!; isotype, NY!).
А member of the genus Orthosia because of its
basally fused corona and adaxially glabrous corolla
lobes.

Metastelma sepium (Decne.) W. D. Stevens. Phyto-
logia 604: 335. 1988. Vincetoxicum sepium Dec-

ne.. in A. P. de Candolle. Prodr. 8: 526. 1844.
Cynanchum tipi (Decne.) Standl.. Contr.
U.S. Natl. Herb. 23: 1177. 1924. TY PE: Mex-
ico. Oaxaca: in hac 2300 m, Н. G. Gal-

eotti 1533 (holotype. Pl; isotypes, Gl, K!).

A member of the genus Orthosia because of its
basally fused corona and adaxially glabrous corolla

lo yes.

INSUFFICIENTLY KNOWN NAME

Metastelma selerianum Schltr.. Bull. Herb. Boissier
6: 841. 1906. TYPE: Mexico. Chiapas: Cerro
de Tonalá. "in pratis montanis." Feb., C. Seler
& H. Seler 2056 (holotype. В destroyed).
In contrast to Metastelma lanceolatum. no spec-

imen annotated “Metastelma — selerianum™ by

Schlechter or anyone else was found, and the de-
scription gives no hint as to the identity of the tax-

on.

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Albers. E & U
\sclepiadoideae.
and e -volutionary б е within Apocynaceae s.l.

Missouri Bot. 24—050.

mima & n Mev ve, 1990. IOPB е И

some hii 2: Asclepiadaceae. ТОРВ Newslett. 15: 11—
| 4.

Bartlett. H. H. 1909, VII. Descriptions of Mexican phan-
товат». Proc. Amer. Acad. Arts 44: 630-037.

„ 1844. In: R. B. Hinds (editor), The Botany
f the Voyage of H.M.S. ا‎ Smith. Elder, London.

Blankinship. J. W. 1907. Plantae

III. Annual Rep. Missouri Bot. can 123-223.

Brown. R. 1810. On the Asclepiaeae, a Sale Order of
Plants Separated. from. the кок of Jussieu. R.
Brown, London.

Chaturvedi, S. К. 1988. Abiotic M tion in p
hirsuta Wight (Asc "reis skle epi 93-02.

D A cy, W. G. 1987.

Meve. 2001. A karvological survey of

Periplocoideae and Sec E ае.

=j
=

—

. Par

a of Panama—C hecklist ui чуя * Pari 1: “The Intro-
u tion and Checklist. Monogr. Syst. Bot. Missouri Bol.

LE:
Decaisne M. J.
à due ^ 1
p Vol. 8. Treuttel. Wü
Fishbein, M.
Martin, D. "i
T. R. Van Devender & R. Wilson b mw E mir s Río
Mayo a Univ. Tucso
R. Levin.
cle q ae): A new
the status of Basistelma Bartlett.
Fournier, E. 1885. Ascle TE eae. In:
tius (editor), Flora > ie n ‘nsis, Vol.
pographia Regia, Müncher

Notes on Cynanchum (Asclepiada-
О.

‚ Asclepiadaceae. Pp. 490-084 in A.
Prodromus Systematis Naturalis
P:

^

Arizona Press
1997. Me ie in mexicanum (As-
combination and re-e ores "i
е 14: 208-2
^P von e
ae 298. Ty-

Henrickson, J. 1987.
ceae). Sida 12:

Hewson, Н. J. 1988. Plant indumentum—A hi mdbook of
к, Austral. Fl. Fauna Ser. 2: 1-2
Kunze, H. 1991 poe EN and function in asc da ‘piad pol-
E D Syst. Evol. 176: 227-253.
19

. Corona нер nectar system in Asclepiadi-
nae (Asc ا ا‎ eae). Flora 192: 17: 3
8

Levin, G. X. & огап. 1989, Asc le din eae: Rubi-
aceae, The Vascular Flora of Isla Socorro. Mexico. 16
ed.: 26; 50-51. Society of Natural History, San Diego.

Liede, S. 1996a. Sarcostemma (Asclepiadaceae =A con-
troversial generic. circumsc 5 reconsidered: Mor-
P m л idence. Syst. Biol. 3144.
— \ revision E Cma |
cei РЕ! in и а. Ann. Missouri Bot. Gard. 83: —
1997. Subtribes and genera of the tribe
CN (i чч ynaceae—Ascle spiadoida ae)—A synopsis.
pu M 241.
i rs. 1994. Tribal cr np of Asclepia-
daceae ge nera. Taxon 43: 201—2:
.unze. 2002. un and the Cynan-
chinae (Apocynaceae—Asclepiadoideae)— A molecular.
anatomical and latex triterpenoid study, Organisms. Di-
versity Evol. 2: 239-209.
A. Täuber. 2000.

Ascle к

Asc de.

Ree

Sarcostemma R. Br. (Apocy-

84

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naceae—Asclepiadoideae)—A controversial generic cir-
cumsc jose às с EET E : bae е from trnL-F spac-
rs. P ).

vol. 25:

& 0 ircumscription of the genus
Cynanchum (Арес упас раг ‘lepiadoideae). Syst. Bot
301.

Lumer, C. . Yost. 1995. The reproductive biology
of Vincetoxicum nigrum (L.) Moench (Asclepiadaceae),
a Mediterranean weed in New York State. Bull. Torrey

Pome

Asclepiadaceae, Atlas of Medicinal
и of Middle Хей ica: MN to Yucatan. Charles
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BL Н. F. 19 ae—New or interesting

le aM 13: 96-116

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hs Gerais, Brasil. Bol. Bot.

Univ. Sao Paulo 19 169.

‚ М. W. Chase, b. J. Goyder & J. Griffiths. 2003.
eae classification: Evaluating the phylogenet-

World Asclepiadoideae (Apo-

Адорна
ic no of New
cynaceae). Taxon 52: 33-50,
Salvin, 0. 1869. A synopsis of p сеш Clothilda. Trans.
Entomol. Soc. uer 675 397.
Schlechtendal, D. E Hora Insulae Sti.
India Occidentalis. iue : 722-7 =
33. De plantis mexicanis A. G. Schiede M.
e. collec v шо adfert. Li o 8: 513-528.
Se hlec he H. ). Ascle р ас pe i: 1. Urban ety
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1906. Asc ed Herb. Boissier 6:

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"Bull.

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Schumann, К. 1895. Asclepiadaceae. /n: A. Engler & К.
Prantl lior p natürlichen Planzenfamilien. Vol.
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Shinners, L. H. 1952. нан grayi Shinners nom.
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. 1964. Texas Asc E СЯ eae other than Asclepias.
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Standley, P. J Apocynaceae;

U.S. a Herb. 23:

Asclepiadaceae.

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19 e Asclepiadaceae. Pp. 177-17
Standley Calderón (айй), Lista 1 de

las e de El Salvador. Tip la Union Dutriz her-
manos, pe Salvador.
8a. Asc Vide ee In: Flora of Honduras.
Publ. Field ib Nat. Hist., Bot. Ser. 17: 387-388
. Ase Vial eae. /n: Flora of Costa Rica.
Publ. re Mus. Nat. Hist., Bot. Ser. 18: 949—960.
Record. 1935, Asclepiadaceae. In: The
Мену ae flora of British 1 Publ. Field Mus.
Nat. Hist., E )-331
Stevens, W. D. New names and saree in
Apocyneae, * 1 ae. Phytologia 64: 333-335.
———. 2000. New and interesting E И (Apocy-

naceae, Ascle HEN n Novon 10 v ds
—— ———. 2001. Ascle e eae. In: W. ens, C. Ul-

O. M. Montiel ics Flora de
0. Monogr. Syst. Bot. Mis-

loa Ulloa, A. Pool & &
Nic 'aragua, Tomo 1: 234-27
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Sundell, E. 1994. Asc Vʒ‚p аи family. J.
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Thomas, A. V. & Y. Dave. 1991. 5 and phy-
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1986. Part И (6): Collectors "S." In: F. R.
Stafleu Бао). Index Herbariorum. The Hague.

Weberling. F. 1989. Morphology of Flowers and Inflores-
cences. ACE Univ. Press, Cambridge.
). New and 1 known species from
the Sonoran 2 8 Contr. Dudley Herb. 3: 65-86.
———. 1980. Asclepiadaceae. Pp. 202- ae in Flora of
Baja California Stanford Univ. Press, Stanforc
Williams. L. . Asc M ri In: Tropical Amer-
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е Tropical American 5 9 XII. Fieldiana,
102.
R. E. 1941. The North American Asclepiada-
. Ann. Missouri Bot. Gard. 28: 193-244.

ooa.

APPENDIX I. Numerical index of species.

la. М. arizonicum subsp. arizonicum
lb. М. arizonicum subsp. chiapense

2a. M. barbigerum var. barbigerum

2b. M. barbigerum var. m
2c. M. barbigerum var. veracruzens

За. M. californicum e ы ш
ЗЬ. M. californicum subsp. lanceolatum
4. M. cuneatum

5. М. eliasianum

6. M. latifolium

7. . longicoronatum

8. M. mexicanum

9. M. minutiflorum

10. M. palmeri

11. V. pedunculare

12. M. pringlei

13. V. schaffner

l4a. M. schlec endi var. schlechtendalii
14b. М. schlechtendalii var. arenicola
14c. M. schlechtendalii var. trichophyllum
15. M

, . Stenomeres
16. М. turneri
APPENDIX 2. Index to collections examined.

The numbers in parenthe ses refer to the corresponding
species in the text and in the Numerical List of Species
presented above in ie dix 1.

Aguilar 124 (14a); Albers Е al. 46448 (2а); Andréz
кеже, & Carranza 1111 ; Aspra 65 (14c).

Jarkelew 217 (3a); Bakley 13360 (2a): Barkley et al.

155 (2a); Barlow 28/17 (2b); Bennett et al. 646 (12);
жш s.n. (За); Berlandier s.n. (14a); Blake 7793 (1b);
Boege 862 (3b), 1301 (2c), 1438 (3b); Brandegee s.n. (3a),
(4); Breedlove 14010 (2b), 27183 (7), 27820 (14c), 28258
(14c), 28986 (1b), 62261 (3a), 62528 (3a); Breedlove h
Raven 13199 (7); Breedlove & Thorne 20658 (14c);
2984 (2c); Burgess 5695 (la): Burgess & Van Doce
5235 (12). 7661 (3a); Butterwick 78 (14a).

;abrera & Cortéz 281 (14a); Cabrera & De Cabrera
9505 (14a); Calderón 1271 (14c); Calvert 117 (2a); Car-
ranza & García 1080 (12); о ѕ.п. (2с); Сһаѕе 7418
(3b); Chiang et al. 7527A (10), 7550 (10). 7964 (2а),
8161р (2a), 9015 (12), 9274 (12), 9366a (12), 9501 (12),
11387 (12); Conrad 9319 (10); Contreras 532 (2b), 3068
3866 (14a), 6602 (14a), 7237 (14a), 7270 (14a),
8466 (2b), 9336 (10); Correll 33825 (12); Correll & Cor-
rell 12756 (2a); Correll & Johnston Wee да), 20219
(12); Cowan 3616 (2a); Cowan & Mag 0 (2c); Cow-
an et al. 5: jos (2a); Croft 62 (2a); С! 75 1 1125 (2a),
2984 (2a), )ОО (2a).

Tae hie 406 (2b); Davidse & Brant 32667 (14a);

Volume 91, Number 1
2004

Liede & Meve 85
Revision of Metastelma

Davis & ое 66297 (3a); Dorantes 5270 (2с); Dorr
2359 (1( 16); Drees et al. 74-15 (la): Duke 12414 (5)
Dwyer 2800 (5).
Edwards s.n. (2b); \
(11); Engard & Getz 331 (12): Engard & Gentry 686 (12):
Ertter 4906 (2a). 5357 (2a).
Felger 9579 (1a), 9635 (3a), 15588 (1a); Felger & к;
үт 15620 (la) Felger & Quijada-Mascarenas 91-3:
: Felger & Schne idis 95-84 (la): Felger & E
A | (la), 84-490 (la); Fernández 4731 (ЗЬ): Fernandes
& Barkley 14485 (2a); Ferris 8589 (3a); Fishbein 2400
(6). 2759 (4); Fishbein & McMahon 2750 (3a). 2709 (3a):
SH ein et al. 1362 (8), 1448 (8), 1606 (6),
1903 (6). 1905 (6): Flügel & Geiseler 7016 (14a): Fried-
man 015-95 (4), 104-95 (4). 150-95 (4). 199-95 (4). 2
94 . 319-94 (14b); Friedrichsthal s.n. (14a): сид ll
3651 (2, а). 3820 (16); Fryxell & Anderson 3617 (3b)
Galeotti 1571 A (3b); Gaumer 539 (2b). 23436 (14a).
24230 (14а); ди 1508 (2b). 1755 (15). 2517 (Ab):
Gentle, P. H. (15), 3815 (14a). 4190 (15). 8458 (15):
Gentry 1098 TR 1298 (la). 2373 (6). 4857 (9). 5184
(13), 5431 (14b), 5479 (13), 5562 (13), 6723 (2a). 7136
(3a). 7438 (3a). 7716 (3a). 14304 (la), 14466 (la): Gentry
& Engard 23247 (12); Ghiesbreght 664 (1b): Gilman | 10
(la): Ginzbarg 131 (10); borde 76-322 (6); Goodding
116-45 (1a); 208-45 (1а); Gould et al. 2804
man 386 (2b): Gregg s.n. (2a): ee 1632 (2b).
14a).
Haber 615 (11); Hall 521 (2а); Harmon 4189 (11); Har-
tweg 601 (11); Hastings & Turner 67-64 (3a); Haynes &
Stewart s.n. (За); Heller 1559 (2a); Henrickson 6100 (12).
6366h (12). 6427 (12). 7891 (12). 11497 (12). 11724 (10).
12070 (12). 12481 (12). 12980b (12). 19138b (12). 19303
(2a), 20400 (12); Henrickson & Lee 17559 (2a): Henrick-
& Prigge 15352 (12): Henrickson € Wendt 12028
: Hernandez 1534 (16): 1562 (2a). 1917 (12). 1940
: Heyde & Lux 3060 (14a). 0348 (14а): Hill 10627
(10): Hine kley 2105 (12), 3106 (12), 3954 (10), 4088 (10):
Hinton 17660 (12), 17776 (16). 23343 (12): Hinton el E
1310 (3b), 19616 (12), 19732 (2a), 24186 (2a), 242
(2a): Howell cogo За).

—
~

с =
Se =.
ш.

—

=

=,

la): Green-
5462

11): Johnston, 1. М.

Jenkii -88 (8): Jimenez 26 17 (
8438 (12) Nu I. M. & Muller 261 (12). 834 (12).
950 (12); Johnston. M. С. 4369 (10). 5063B (2a); John-
ston, M. г & Graham 4525 (2a). 4674 (2a): Johnston. М.
et al 157A (12). 11991 (10), 12077 (12). 12125B

Keil 4323 (la): 2 & Smith 14531 (5).

LaBounty et al.! 12); Lavin et al. s.n. (12); Le Roy
s.n. (la): Lehto е P Lemus 11 (12); LeSueur 361
(10): 1053 (12): Liede 3242 (2b): Liede & Conrad. J. 2557
(7). 2004 (13). 2610 (2а). 2612 (10). 2613 (10), 2955 (За).
2961 (13), 2962 (13); Liede & Meve 2500 (2a). 2501 (12):
Lindheimer E а, 992 (2a) Lundell 651 (14a). 3502
(14a). 5517 (12). 6050 (15). 8734 (2a). 16709 (2b). 17022
205 L dun 11 : t m 118113 (14а).

1 116 (116): Machuca 7400 (3b): Marsh
: Martin s.n. (За); Martin & Mc-
Д sey 3034 (13). 14284 (146); Mar-
5 (2a): Matuda 3765 (2b); McGee
.n. (12); О n & Bowers 2119
(3a): Modos & Mé ant 2566 (10); Mendraño 1630 (13);
51 (14a); Molina 3 (1b). 13162 (Ib).
Pee (14c). 13344 (14c). 13370 (14).

155 (14c). 18607 (14c). 22438 (14а),
a). rs (11): Molina & Molina 24843 (11):
Moore Jr. & Wood Jr. 4409 (3b). 4259 (3b): Moran 9141

(9); Moser et al. 18152 (la) : Mueller, C. Н. 2099 (16),
8115 (12): 1 sr, C. H. & Mueller, M. T. 188 (16): Müll-
er, F. 1853 a
& d зе 10076 (la): Nesom et al.
5957 (10) Nixon & Cowan 831 (3a).
O'Neill 8659 (2b). 8660 (s "

Palmer 159 (13), 22: . 360 га, 626 (la). 665 (6).
824 (10). 828 (10); Panero & Calzada 4026 (10). 4040
(10): Patterson 647 6 (16), 6519 (2a): Pennell 10220 (2a).
10320 (2a), 17729
3539 (5): Pringle 70 (12), 9
2836 (2а), 3138 (3b). 4766 (13).
6646 (2a). 6706 (10). 10838 (3b). 1 yes (13), 11841 (16).
s.n. (la): Purpus 1259 (13), 2094 (2c. 14a). 2617 (13).
3244 (10). 7273 (Ib). 9078 (Ib), 9167 (3b). 9169 (1b).
10217 (Ib).

Reeves & Pinkava 13075 en Reina et al. 96-286 du
in 1087 (6); Reverchon 1558 (2a); Rodríguez 1024 (12

{ое & Roe 1885 (3b); Roe et al. 997 (14c): Rose 1
: vr 1218 (12); = Il et al. 11402 (la). 11584 (la).
. 12115

7592 (2a).

=
دن‎
=
c
—
a)
Ф
Ф
N
^^
ее
oy А
pend
=
2
їл
mm
Э:
—
=
ás
5

00 & Tenorio 3294 (3b): Sand-
ers 9265 (14b); Sauer & ire 3137b (2b): = rs 740
(Ida): Schaffner 652 (13); Schiede 11 (14a), 159 (14a).
200 (14а); Schipp 674 (1 5) Shortman 90-27 s ‘Shre "se
6468 (3a). 7197 (3a), 8417 (2a X "y 312 (3b); Shreve
& Tinkham 9694 (12): Skorepa 173 b Skutch 1438
(14а); Small & Wherry 11875 (2a): si M124 (2a); So-
corro Gonzales 840 (12): Sousa et al. 10929 (14a); Stan-
ford et al. 68 362 (12). 920 (NY id (16): Stein-
mann 955 (6). 03-358 (14b). s.n. (6. 8

Varela 972 (la): Spellenberg & Re Des 5353 (8): Stevens
1250 (14a). 1: “es (2с); Stevens et al. 2259 (10). 2260 (10):
Stewart 466 (12

Taylor, J. & Taylor С. 11393 (11), 12532 (2c);
М. 172 (12); Taylor. R. J. 4251 (11). 4285 (11): Tenorio
. 7660 (13), 10441 (3a); Tharp, B. C. 248 (2a),
(2a). s.n. La): Thomas & Felger 11785 (1a). 11942 " a)
Ton 1548 (14c). 3092 (14c): Tonduz s.n. (Herb.
(11): Torres & Garcia 6656 (10); Tourney s.n. (Та); Тип
m ot (14a). 1494 (14a); Turner, B. L. s.n. (13): buts
H. & Hastings 64- E (14b): К. М. et al. 79-
ve na Tyson et al. 2 (5).

Van Devender & UE s.n. (8); Van Devender & Reina
98-1132 (la): Van Devender & Yetman 94-698 (1); Van
Devender et al. 92-121 (3a), 92-133 (4), 93-1253A (4),
93-1265 (4), 93-1284 (4), 93-1310 (la). 93-65 (la). 98-
1285 (9), 95-1189 (6), 84-29 (la). s.n. (8): Vilasefior el
al. 1621 (12): Villarreal & Carranza s.n. (16):
et al. 3115 (2a).

Wagner et al. 4120 (12): Warnock 21851 (12): Wawra
625 (1 aa) Webster & Webster 119 (2a); Webster & Wilbur

): Steinmann &

Taylor,

‘Turner,

Villarreal

3060 (2a): зу et Е 2 (10): White. D. & Mott 74
(3b): White. 5. 3239 (13): Wiggins 7191 (9), 7491 (la).
15048 (За), : 508 5 dm 15628 (13): Wilson 11388 (10):
Woodson et al. 1263 (5). 1499 (5), 1500 (5): Wright 1676

(2a). 1077 e s.n. (2а); Wyatt 1464 (2a); Wynd & Mueller
26 (12), 244
S. coll. ым bl 3198 (2a).
APPENDIX 3. Index to scientific names.
Astephanus pubescens Greenm.
Basiste Ima 1 (Jorr. ' an 1t 61
randegee) Bartlett €
Cynanchum arizonicum (A. Gray) 8 39

barbigerum (Scheele) Shinners 43

86 Annals of the
Missouri Botanical Garden

barbigerum (Scheele) Shinners var. breviflorum Shin- barbigerum Scheele var. veracruzense Liede &
Meve 46
californicum (Benth.) Moran 47 californicum Benth.
chiapense (А. Gray) Standl. & Steverm. 42 californicum Benth. subsp. californicum 47
collinum (S. F. Blake) Standl. & eig 42 californicum Benth. subsp. lanceolatum | (Schltr.)
Liede & Meve 49
5 A. Cray 42
num S. F. Blake
5 Brandegee 52
decipiens Pittier 73

ners

y 3:
filisepalum (Standl.) L. O. Williams 82
glaberrimum (Woodson) L. O. Williams 82
grayi Shinners 63

infimicola L. O. Williams 54 eliasianum Dugand 54
liesnerianum L. O. Williams 46 eulaxiflorum (1 un 1 iede 82
эш oronatum L. O. Williams 57 filisepalum Stam
maccartii Shinners var. latifolium Turner ex Henrick- glaberrimum Age -
son 80 infimicola (L. O. Wiliams W. D.Stevens 54
maccartii Shinners var. maccartii 63 lanceolatum Schltr. 4
miserum L. O. Williams 8: latifolium Rose 57
palmeri (S Satan) Blake 04 liesnerianum (L. O. Williams) Liede :

longicoronatum de O. Lo lliams) L le « Meve 57

sc Fu ы (Decne.) Standl. & Steyerm. 73
sepicola (Pittier) L. O. W = 66
sepium (Decne.) Standl. ¿

miserum (L. O. Williams) W. D. Stevens 83
4

palmeri 5. Watson 63
sonorense Moran 63 xirviflorum R. Br. ex Е һин. 73
* . . he

stenomeres о & Steyerm. 80 je ол. Schltdl. 7:

tric ida di pcd dont L. О. | Williams 77 pedunculare Decne. m

wigginsu Shinners 6 pringlei A.Gray 6

woodsonianum = O. Williams 66 pubescens ones ) W. D. Stevens 83
Ditassa mexicana Brandegee 49 rubens in 12 9 M. D. Stevens 83
Jobinia a undell) W. D. Stevens 82 scha 71

йт сег иЗ De спе

Me linia angustifolia A. Gray 6
schlechtendalii Decne. var. arenicola Liede &

mexicana Brandegee 61
Metastelma oo = 39
albiflorum S. Watson :

Meve 77
schlechtendalii Decne. var. schlechtendalii 73

а Miel üm Tore E Ki eas | us n var. trichophyllum (L.
ми Тигез. 82 ams) Liede бг Meve 74
selerianum Schltr. 83
arizo гау 39 i
"OM Ру sepicola Pittier 66

arizonicum A Gray subsp. arizonicum 39 T

E \ Gray subsp. ehiapense (A. Gray) Lied sepium (Decne.) W. D. Stevens 83

: Cas nba. е e (A. Cravi Liede І |

ечеи т satay suas] I 7:8) “ee stenomeres (Standl. & Steyerm.) W. D. Stevens 80

& Meve 42 trichophyllum (L. О. UA W. D. Stevens 77
barbigerum Scheele 43 turneri Liede & Meve
barbigerum Scheele var. barbigerum 43 atsonianum Standl. E
barbigerum Scheele var. liesnerianum (L. O. Wil- Éatahas angustifolius (Torr. A: = Watson 61

liams) Liede & Meve 46 Vincetoxicum sepium Decne. 83

A TAXONOMIC REVISION OF Hong De-Yuan? and Pan Каг- Yu?
THE РАЕОМА ANOMALA
COMPLEX (PAEONIACEAE)!

ABSTRACT

Based on field observation, examination of over 350 she els of exsiccalae. and investigation of all the relevant types.
a taxonomic. revision of the Paeonia anomala complex is presented. Typifications are clarified for P anomala. P.
intermedia, P. hybrida, P. sinjiangensis. P. altaica, and P. veitchii. The identity of three well-known taxa. P anomala.
P. hybrida. and P intermedia, is also clarified. Two species. P anomala and P intermedia, are recognized, with the
circumscription of P anomala emended to include P veitchii as its subspecies. Paeonia sore includes two sub-
species: subspecies anomala and subspecies veitchii with the former distributed in Central Asia, Siberia. and the
northeastern I uropean part of Russia, while the latter occurs in China southeast of the Gobi rm Porania intermedia
is distributed in Central Asia. but with an isolated locality in Georgia. Paeonia sinjiangensis is treated as a synonym

L. The

of P anomala, and P. hybrida Pallas is treated as a synonym of P. tenuifolia > lectotypes of Paeonia laciniata.
Paconia beresowskii, and Paeonia intermedia are designated here in the present paper.
Key words: Paeonia, Paeonia anomala complex. Paeonia hybrida. Paeonia intermedia, Paeoniaceae.

The Paeonia anomala L. complex (Paeoniaceae) needed a comprehensive taxonomic revision and
comprises a group of herbaceous peonies in Central review of the nomenclature. For this purpose, the
Asia. Siberia. and adjacent northeastern European first author examined all available specimens of
regions. They are characterized by leaves biternate this group in the herbaria at BM. HNWP. K, LE.

with leaflets decurrent at the base, leaflets finely NWTC. PE. SHI. SHMU. TBI. XJBI. XJNU. and
segmented. with segments of a lower (the best de- NJU (see Appendix 1). In addition, the types of PF

veloped) leaf ranging from 70 to 100 in numberand anomala. P. hybrida, P. intermedia, and the other
4-32 mm in width, and by bristles along veins on six specific and varietal names were examined
the upper blade surface. The only species with LINN (Herbarium of the Linnean Society). BM. К.
which it may be confused is Paeonia tenuifolia |... and PE. respectively.

but the latter has leaves even more finely seg-

mented. with segments more than 130 in number HISTORICAL REVIEW

and 0.5-6 mm in width. ps

* pi eE Within the Paeonia anomala complex the type
Since the late 1970s. two new species in the : : м ES
› | species, P anomala, was described from Siberia by
Paeonia anomala complex have been described д ih à i : :
. ere i . пра , Linnaeus (1771). Pallas (1789) described three ad-
from Xinjiang, the Central Asian part of China: P
sinjtangensis К. Y. Pan (1979) and P. altaica K. M.
Dai & T. H. Ying (1990). For a better understand-
ing of the species group in Xinjiang, we made an

ditional species, P. laciniata and P. sibirica from
Siberia. and P hybrida from a plant raised from
seeds of P. tenuifolia cultivated in the Botanic Gar-
Su. x den of the St. Petersburg Academy in Russia.
expedition in 1993 to the Altai and the Tienshan „ dat MR 8 е

: Paeonia sibirica Pallas (1789) shares an illustration
in Xinjiang and found that morphological features ars os
(tabula) with Р, laciniata, but does not have a de-
of the group in Xinjiang were not consistent. with
the N by Schipezinsky (1921, 1937) and
Gamaulova (1961); Stern’s (1946) treatments and

nomenclature are different from theirs but do not

scription. In his monograph of Paeonia, Anderson
(1818) recognized only P. anomala, reducing P. hy-
brida as a synonym of P. tenuifolia for the first time.
De Candolle (1818) recognized P anomala. P. hy-

reflect the reality of the group in Xinjiang, either. : x
р de J brida, and P. laciniata, but later (1824) treated P

Thus. we realized that the P anomala complex

The authors are grateful to the National Geographic Society for financial support (Grant 6408-99), which allowed
us to examine herbarium specimens at the Komarov Institute of Botany, the Russian Academy of Sciences. and to
conduct fie е in Georgia. The project is also supported by the Nat ional Natural Science Foundation i i hina ( NSEC
Grant 30130030). We are grateful to the curators of the following herbaria: BM, НМР, N. LE. N „EE, SEI.
SHMU. i XJBI. XJNU. and: XJU. We sincerely thank Zhou iang for his assistance with fie VE pet li Ol 10-
Ling and Ma Li-Ming for their help in preparation of the manus
Laboratory of Systematic and Evolutionary Botany, Institute of M The Chinese Academy of Sciences, Niang-
shan, Beijing 100093, China. hongdv(Ons.ibcas.ac.cn

ANN. MISSOURI Bor. GARD. 91: 87-98. 2004.

88 Annals of the
Missouri Botanical Garden
laciniata as a synonym of P anomala. Meyer riety anomala and variety intermedia (Pan, 1979).

(1830) described the fourth species, P. ae
from the Altai Mountains. Ledebour (1842) cite

anomala, P. hybrida, and P. intermedia, is 5
laciniata as a synonym of P. anomala. Trautvetter
(1860) recognized only one species, reducing P. hy-
brida as a variety of P. anomala, and treating Р.
intermedia as a form of variety hybrida. Lynch
(1890) cited P. hybrida and P. anomala, and stated
that the former was native to the Caucasus. Huth
(

omala,

892) adopted the widest species concept of P. an-
which includes four varieties: var. typica,
var. hybrida (= P. intermedia), var. nudicarpa, and
var. emodi (— P. emodi, confined to the western
Himalayas). A further treatment by Krylov (1901)
divided the complex into two species, P. anomala
and P. hybrida, and reduced P. intermedia as a va-
riety of the latter, P. hybrida var. intermedia (C. А.
Meyer) Krylov, in addition to the typical variety. In
the area of West Tienshan (Kirghizia and Xinjiang.
China), Trautvetter (1904) enumerated only P. an-
omala, treating Р. intermedia as its subspecies.
Schipezinsky (1921) basically followed Krylov
(1901), recognizing two species, P. anomala (with
two varieties, var. anomala and var. nudicarpa) and
P. hybrida (with two varieties, var. hybrida and var.
intermedia), and the same treatment was adopted
for the Flora of the USSR (Schipezinsky, 1937)
These two Paeonia species were grouped by him
as series 4, Dentatae Kom. (Schipezinsky, 1937: 33,
"leaf lobes incised or with dentate margin"). Roots
of both species were described as tuberous. In con-
trast, Stern (1946) recognized only one species in
his monograph of Paeonia, P. anomala, in which
two varieties were recognized: variety anomala with
glabrous carpels, and variety intermedia with to-
mentose carpels. He did not mention roots of this
946: 113) considered P. hybrida Pal-
las as an ambiguous name: “It is doubtful what

group. Stern (

species Pallas intended by this name and, as it is
not possible to discover what he meant, this name
of P. hybrida has been omitted." However, in the
Flora of Kazakhstan, Gamaulova (1961), following
Krylov (1901) and Schipezinsky (1921, 1937), de-
scribed two species, and still recognized P. hybrida
as a valid name.

While working on Paeonia for the Flora Reipub-
licae Popularis Sinicae, Pan (1979) found a speci-
men from Xinjiang whose roots were basipetally at-
Schipezinsky (1937) and
Paeonia anomala and P. hybri-

tenuate. According to
Gamaulova (1961),
da have tuberous or fusiform roots, so the plant was
described by her as a new species, Р. sinjiangensis

. Y. Pan; the plants with tuberous or fusiform roots
were treated as P. anomala with two varieties: va-

Also from Xinjiang, Dai and Ying (1990) described
another new species, P. altaica, which was stated
to have flowers larger than P. sinjiangensis and one
or two underdeveloped flower buds in addition to
the terminal blooming flower.

Interestingly, Schmitt (1999) failed to recognize
the distinct differences between Paeonia anomala
and P intermedia in the root and calyx, and thus
treated them as a single species, but still recog-
nized P. sinjiangensis and P. altaica as distinct spe-
cles.

From the above it is clear that Paeonia hybrida,
P. intermedia, and P. anomala have been variously
treated. With this paper we hope to clarify the bi-
ological attributes and variations of the P. anomala

complex.

OBSERVATIONS AND DISCUSSION

To answer how many species were really present
in Xinjiang and what biological features they have,
1994)

made an expedition to the Tienshan and Altai

the first author and coworkers (Hong et al.,

Mountains, conducting field observations and pop-
ulation samplings of Paeonia in 1993. Seven pop-
ulations in total were observed, covering those
character states previously described for the P. an-
omala complex (Table 1). We found there were only
two species in Xinjiang that differed distinctly from
each other in the root and calyx. One species had
the roots basipetally attenuate (carrot-shaped) and
sepals mostly caudate (Fig. 2), preferring relatively
moist habitats in woods. This was treated as P. sin-
Jiangensis. The other had roots tuberous or fusiform
and sepals mostly (at least 2) rounded but not cau-
date at apex, growing on sunny, shrubby or grassy
slopes, or in sparse woods. This latter was recog-
nized as Р. anomala. We also found the presence
or absence of indumentum on the carpels in this
species group to be a polymorphism, i.e., individ-
uals with carpels either glabrous or from sparsely
to densely pubescent could be found within a single
population (Table 1). The indumentum on carpels
was demonstrated as quite variable, although it was
considered by the previous authors as taxonomi-
cally valuable. Therefore, any taxonomic division
based on this character, such as that between P.
anomala and P. anomala var. nudicarpa (by Huth,

2) «

co

` P. anomala and P. anomala var. inter-
media (by Stern, 1946), is artificial. Also not ob-
served by the previous authors was the clear dif-
ferentiation in root and calyx in this group. which
are closely correlated with each other (Fig. 2).

We also found that in the form with carrot-shaped

Volume 91, Number 1
20

Hong & Pan 89
Paeonia anomala Complex

Table 1.

character states, while those in parentheses indicate the number of individuals observed. The indumentum on carpels is divided more or less arbitrarily into six grades with “О”

The populations sampled and their characters in the Paeonia anomala complex in Xinjiang, China (all the vouchers are in PE). The figures before parentheses indicate

“1” extremely sparsely hairy, “5” entirely covered with hairs, while 72," “3,” and "4" are in between.

ssing totally glabrous.

>

ехрге

Ind umentum

Number of
non-caudate sepals

on carpels

0(2); 101);

Leaf color

Roots

Altai: Mt. Halamaryi, NW of Altay City, 1

Locality and habitat

Population

D. Y. Hong et al. 3

5(1)

e

pale green

carrot-shaped (3)

200 m, Pop-

ulus forest by stream

Altai: Xiaodong Gou Valley, NE

00)

carrot-shaped (3) pale green

m, Populus-Betula-Picea forest at valley bottom

of Altay City, 1060
Altai: Habahe County, 1200-1550 m. in Betula forests

4

D. Y. Hong et al. 5

4): 0(2)

—

0

T. H. Ying 1006—1022

D. Y. Hong et al. 2

'arrot-shaped (2)
fusiform to tuberous (3)

2(1): 3(5)

0(1):

20): 3(5)

green

.

Halamaryi NW of Altay City. 1300 m, S

slope, rocky Berberis-Spiraea bushes
Altai: Mt. Halamaryi, NW of Altay City. 1000 m.

Mt.

Altai:

green

fusiform to tuberous (2)

5

D. Y. Hong et al. 012

sparse bushes
Altai: Xiaodong Gou, NE of Altay €

green 3(2): 41) 0(1): 5(8)

fusiform to tuberous (6)

4

D. Y. Hong et al. 4

ity, 1060 m. W

slope, rocky sparse Spiraea-Berberis bushes
Tienshan: Yining County, Yining Forest Farm, 1150—

2(4): 3(1)

green

fusiform to tuberous (5)

D. Y. Hong et al. 1

1200 m. N slope. sparse Prunus-Malus forest with

Cotoneaster & Spiraea

roots, the petals varied greatly in length, from 3.5
to 6.5 em, and in the Altai Mountains some indi-
viduals of this form possessed one or two additional
underdeveloped flower buds similar to Paeonia
veitchii. This was again a polymorphism. and not
considered by us to be a stable character, and
therefore P. altaica was reduced to a synonym of P.
sinjiangensis (Hong et al., 1994).

ler examination of about 200 sheets of her-
m specimens in the Komarov Institute of Bot-
any (LE) in 1999, the first author found that two
species could also be distinguished in this complex:
one with the roots carrot-shaped and sepals mostly
caudate. while the other with the roots tuberous or
fusiform. and sepals mostly non-caudate. These bi-
ological features match those on plants observed in
Xinjiang (Hong et al., 1994). Gamaulova (1961,
tab. 2) described roots of Paeonia anomala as fu-
siform-thickened, and those of P. hybrida as tuber-
ous-thickened. However, roots of P. intermedia (—
P. hybrida sensu Schipezinsky and Gamaulova)
vary in shape from tuberous consistently to fusi-
form, and this variation could be found within pop-
ulations or even on the same individual, whereas
in P anomala neither fusiform-thickening nor tu-
berous-thickening were found.

Contradictions exist between our natural obser-
vations (Hong et al., 1994) and earlier descriptions
by Schipezinsky (1937) and Gamaulova (1961).
Stern's (1946) treatment of this complex as one spe-
cies with two varieties (Р. anomala and P. anomala
var. intermedia) is also at variance. For a clear tax-
onomic revision and correct nomenclature, one re-
maining issue ought to be resolved: the identity of
Paeonia anomala, P. hybrida, and P. intermedia.
The type specimen of P. anomala, with two visible
sepals both caudate and relatively thin leaves. is
perfectly consistent with the form with carrot-
shaped roots. According to the type specimen at
LINN [Siberia, no. 692. 3], fi

examination of over 350 sheets of exsiccatae, Р.

eld observation, and

sinjiangensis and P. altaica should be treated as
synonyms of P. anomala; the descriptions of roots
of P. anomala by Schipezinsky (1937) and Gamau-
lova (1961) are erroneous. The type of P. hybrida
(at BM), on which Pallas's (1789) tab. 86 was ap-
parently based, has leaf segments 3—4 mm in width.
and at least more than 100 in number, and is thus
within t of variation in Р. tenuifolia L.

(Hong & Zhou. 2003) "Therefore. P. hybrida Pallas
should be treated as a synonym of P. tenuifolia, as
Anderson (1818) suggested nearly 200 vears ago.
The type specimen of P. intermedia at K possesses
tuberous roots, mostly non-caudate sepals. and rel-
atively thick and narrow leaf segments. The plants

90

Annals of the
Missouri Botanical Garden

that have tuberous or fusiform roots, are distributed
widely from the Altai to Tadzhikistan and Uzbeki-
stan, and were named P. hybrida by Schipezinsky
(1921,

this type specimen very well.

1937) and Gamaulova (1961) correspond to

Stern’s (1946) statement concerning the name of

Paeonia hybrida is not correct, confusing P. inter-

media with P. anomala. Pan's (1979) treatment of

the P. anomala complex (a new species, P. sinjian-
gensis, and P. anomala with var. intermedia) is also
unjustifiable. Although Hong and his coworkers
(Hong et al., 1994) properly described two species
and clearly stated their morphological and ecolog-
ical differences for this group, the nomenclature
they used is misapplied.

The Paeonia anomala complex comprises two
species: Р. anomala and P. intermedia. Paeonia
emodi, which was treated as a variety of P anomala
by Huth (1892), remains a distinct species, with
leaves ternate, without bristles on the upper sur-
face, leaflets much less segmented, segments no
more than 40 in number and 1.54 cm wide. car-
pels usually two, less frequently one, very rarely
three, and flowers white. Paeonia veitchii Lynch
was described from Sichuan Province, China
(Lynch, 1890), and was said (Stern, 1946;
1979) to differ from the P. anomala group in having

Pan,

several flowers instead of a single flower on a stem.
According to our observation, one or two under-
developed flower buds sometimes also exist in ad-
dition to one normal and terminal flower in P. an-
omala, while P.
solitary (P. veitchii var. uniflora), although it has З

veitchii sometimes has flowers
or 4 flowers or 1 to 3 underdeveloped flower buds
in addition to the terminal flower on a stem. Thus,
P. veitchii was reduced to a subspecies of P an-
omala (Hong et al., 2001)
KEY TO THE PAEONIA ANOMALA COMPLEX
la. Roots carrot-shaped, never tuberous or fusiform:
sepals all or mostly caudate, less frequently one
or very rarely two P. anomala
2a. Flowers s r 2 underdevel-
oped flower buds present in SN to ler-

=
=
1
5
ш
=
E
ш

minal flower on а stem
la. P. anomala n ve а
Flowers usually 2 to 4 on a stem or 1 to 3
underdeveloped flower buds present in ate
rarely flowers sol-

=

dition to terminal flower,
itary yn a stem

.P animals 1 veitchii
Ib. Roots fusiform or tuberous; inner 2 te
rounded but non-caudate at apex 2.

sepals

|
P. intermedia

TAXONOMIC TREATMENT
1. Paeonia anomala l.. Mant. 2: 247. 1771.

TYPE: Siberia, no. 692.3 (holotype, LINN!).
Figure 1A.

Paeonia laciniata к аз, Fl. Ross. 1(2): 93, tab. 85, sub
P

sibirica, 1789. TYPE: the illustration (tab.) cited
the аа (lectotype, designated here!).
Paeonia sibirica Pallas, Fl. Ross. 1(2): tab. 85. 1789.

Pallas's (1789) illustration (tab.) 85 has only one
name, P sibirica, and apparently he used this il-
lustration also for P. laciniata because one sees
"Paeonia laciniata Tab. LXXXV" on p. 93. Paeon-
ia laciniata was described in detail by Pallas, but
no description of P. sibirica was given by him.

Perennials: tap roots = 50 em long. carrot-
shaped, basipetally attenuate, up to 2 cm diam.,
lateral roots slender, neither tuberous nor fusiform.
Leaves biternate; leaflets finely segmented; lower
leaves with segments 70 to 100 in number, 8-32
mm in width. Flowers solitary or 2 to 4 on a stem,
often only terminal one fully developed and bloom-
ing; sepals 3 to 5, mostly caudate at apex, rarely
or very occasionally 2 non-caudate; carpels 2 to 5,
from glabrous to densely tomentose.

The species prefers relatively moist habitats,
growing in forests, on the edges of forests, or rarely
in bushes. It is found at altitudes from 1100 to
3870 m.

This species is widely distributed from central
China to the Kola Peninsula of Russia via Siberia
and Central Asia. The species is of two allopatric
subspecies, with the typical subspecies distributed
northwest of the Gobi Desert, while subspecies veit-
chii is in China southeast of the Gobi Desert (Fig.

1а. Paeonia anomala Ll anomala

Paeonia sinjiangensis K. Y. Fl. Reipubl. Popularis
Sin, 27: 603, fig. 12. ao тү! PE: China. Xinjiang:
Habahe County, Larix forests, 1973, Y. R. Ling 1141
(holotype, PE!).

ia altaica K. M. Da „ H. Ying, Bull. Bot. Res.

arbin) 10(4): 33, e n TYPE: China. Xin-

Tank prre County, Wuzliti ti, 1550 m. in forests,

10 June : Н. Ying 1007 (holotype, SHMU;
isolype, pu

The typical subspecies is usually found in de-

ciduous or conifer forests, in valleys, less frequent-

ly in meadows, at altitudes from 1100 to 2200 m.

Apparently it prefers relatively moist habitats. This

subspecies is of very wide distribution: northeast

Kazakhstan, northern Mongolia, from the Altai and

Baikal to the Kola Peninsula in Russia, and in the

Altai and adjacent regions in Xinjiang, China (Fig.

3).

Additional и 5 CHIN
lay, J. R. Xu s.n. Ads. . Halamaryi,

"n Population No. ;

ey, T. H. Ying 7 55 (PE, SHM

Cui 86624 (XJNU). Emin: Shiyue онак. Wuerkehe'er,

ver ag
a Hong «

Hong & Pan

Volume 91, Number 1

2004

Paeonia anomala Complex

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Annals of the
Missouri Botanical Garden

Figure 2.

Diagnostic features of Paeonia anomala (A, В) and P. intermedia (С,

D). Tuberous or fusiform roots are

correlated with non-caudate sepals, while carrot-shaped roots correlated with usually caudate sepals.

right bank of Telikete River, Xinjiang Branch Acad. Sinica

012 (ХЈВІ). Fuhai: Ahebai, glades, s. coll. 3867 (XJBD:

Daqiao Forest Farm, T. H. Ying 1011 (PE, SHMU). Fuyun:

. W. Chang 11356 (ХЈВІ). Habahe: e ae Z. M. Mao

7 75 (XJBD; Tielieke, fea Valley
keli

et al.

Xingfu Town nship, ey, n ju 7305
(XJBD. Qinghe: ш 1 85 ng Valley, Integr. avo
11829 (XJBI). Tacheng: Mt. Ba'erleike, X. Y Li

(SHI). Toli: layer Gold Mine, №. А. Cui 091 е.

Mt. Zayier, N slopes, Integr. Exped. (Biology) pa (XJBI).

Wenquan: Nerxiaoto Gou, А M. Zhang 90-346 (XJNU).
Yumin: Ku'erzhai, Liu & Shen 8308 (XIB I). da
TAN. EE Province: Altai, near Altaiskay

Station, Mt. Narymsky ео gorge slopes, Таду 92
LE). E Altai: Mt. Ivanovs sky Range, near Gorno-
Ulbinki, J. Rohderi s.n. p E). Ustkamenogorsk region: Mt.
Altai, Kunduzda River valley, е 360
(LE); Mt. Kalbinskie, Seryal Day River у | Rezni-
chenko 49 (LE); Mt. Kalbinskie, Ulansky, near Fée ren
by Tainta River, P. Yurchenko s.n. (LE); Mt. Narymsk y,
upper U rkar River, V. Reznichenko 58 (LE); near U Ibinsky
(LE); Urunhaika M mouth, S banks
A. Sedelnikov s.n. (LE). Zaisan region:
Mt. Altai, Ulkunc 1 K River alle ғу, upper Kaldzhir Riv-
er, V. Reznichenko 106 (LE); Markakul Lake, B. Keller s.n.

—
—

>

—
Se
T

LE); Mt. Narymsk y Range, Ak-tui River valley, D. Ya-
же lev 69 (LE);
nichenko s.n. (LE); Mt. S
ley, B. Keller s.n. (LE). MONG OL IA. Ulan Bator: 10 mi.
E of Ulan Bator, P. Morgan 23 (K). Gloucester: Mongo-
Пее nines с Exped. М. P. Price 293 (К). North

. Saldzharsky Pass, E. Klements 11a (LE).
e Region: Altai: between Eu po
balina, mtn. slopes, E. K. Klements ad
Saadak-lary, Vereis 296 (LE).
vennitehny, near Nizhne-U n. S. Kolomoitseva
236 (LE). Buryato-Mongolian Autonomous State:
Baikal, m a s.n. (LE); Zabaikalje, upper
Toreika River, 130 km

W of Troitskosavsk, P. Mihno s.n
(1 Eubinsk R : West Sayan, Mt. Alan Range, Go-
lets Ta Ka I. Krasnoborov 6765 (LE); near Buiba St
tion, by river, ed & Sannikova s.n. (LE). Tuva:

Tandinsky PEN Mt. Tannudla Range, near Shurmak,
V Hanminchun an (LE); Ulug-Hemsky distr., Uiuksky
Mtn. Ran ajan-Kol River valley, Orto- Hem tributary,
Lomonosova & h 'anova 89 (LE). Irkutsk Region: Irkutsk
Prov.: Lena River valley, upper Culm “ay Г Ganda.
LE). lala distr.: near r Bazheevskoye, N. Mal-
tsev 79 (LE). Nizhneudinsky distr.: by Angara River, op-

posite Yandov, 5. in s.n. (LE); Mt. Hariba-bim
Range, Angara River valley, Karpovskoye, A. Korovkin
290 (LE); by Oka River, А. "Krishtofow ihe s.n. (LE); near

~
—
—
=

Volume 91, Number 1
2004

Hong & Pan
Paeonia anomala Complex

Vidimka, Vidim River, S. Kucherovskaya 282 (LE). Tunkin
distr.: Mt. Sayany, near Nylova Pustyn, Y. Komarov s.n.
(LE): Nizhnaya Tunguska valley. near Nizhnaya Korelina,
S. Kokulin 254 ae? Tunkinsky distr.:
Smirnov s.n. (LE). Verholensky distr:

shin ada 179 (LE): Harat, б.
(LE); Lena River & Kirenga valley. Toptykar
67 (LE); Tutura. P. Alexandrov 219 (LE). Kola lin-
sula: Ponoi River, left bank, 8 km from its mouth. E.
Chernov 3 (LE); Ponoi River, near its mouth, V. Orlova
) (LE). Krasnoyarsk Belsk distr.: near Al-
shat. J. Kuznetsov 4661 (LE); Chadobets. G. Borowikow s.n.
(LE): Rybnoe. Dranitsyn & Kochubei s.n. (LE). Enisei
Prov., Achinsk distr.: near Ingol Lake, A. Suhareva s.n.

(LE); near Maloye ree M. Бино а s.n. (LE); Bolshe-
Uluiskaya, near Bobrovki, J. Kuznetsov 53 (LE): тг
River Valley, J. Тиен 247 (LE): Katanga, G. Bo-
rovikov s.n. (LE): Vvezzhi Log. A. Tugarinor s.n. LE.
Kansk distr.: Gutar River valley, by Kamenka tributary.
W. Troitsky s.n. (LE): near Kansk. A. Shliahtin s.n. (LE):
Rybnaya River valley, Perovskoye. J. Kuznetsov 193 (LE):
near Nazimovskoye. Z. Evseeva 4406 (LE). Krasnoyarsk
Prov.: Chunia River, right bank opposite mouth of Mutorai
River, A. Rubin s.n. (LE); Hakassia, Shirinsky distr. Bol-
shaya liusa in valley, с: slopes, Polozhii & iig
sova s.n. (LE): near Krasnoyarsk, by Mohovaya Rive
т skaya & М. "Mishin 104 (LE): Minusinsk. Bols bos
vikul Lake. K. Golubeva et al. s.n. (LE): N izhnava Tun-
dr River valley, near mouth of Hurkakit River, Rubin
& Maskil s.n. (L F): between Salba & Grigorievka, P.
lov s.n. (LE): Shushensky distr. near Tanzyben, by Black
'anzyben River, Kuminova & Alexeeva s.n. (LE): near So-
rokino Station. N slo )pes. Серыя s.n. (LE). Nov osiber-
ia Region: Altai: Elikmanar, upper Karakol River. V. Ver-
eshagin 345 (LE). Kuznetsky Alatau: Kondoma iw
va +A Kazany Mine. Mt. Kyon, B. Klopotor s.n. (LE): up-
per Sary-C humysh River, near Ulus Munai, A. Vydrin s.n.
(LE); Tom River valley, ee owed taiga, B. Klopotov s.n.
(LE). Mariinsky Prov. j. Talitskiebelky,
to Kazanda, Pobe б 697 mE . Lebed River

ime

Кгу-

>

СУ
i"
AC
S
т
=
~.
=
=
-
ES
ч
—

` (LE } i
Сб & Chet River valley, P.

River valley, a & Sabitov s.n.
distr, near Mirny, Lashinsky & Йа ыйа 973
Omsk парон "Tobolsk рилсе: Berezov distr..
ry of Severnaya Sosva. s. re s.n. (LE):
pibe River valley, E. Vislouh 73 (LE).
Ural: Lyapin tributary, upper Manja River,
y гы! have 100 (LE); Severnaya Sosva River valley, Lyapin
tributary, ee Khulga River, B. Gorodkov 512 (LE). Mar-
Beket River valley, Kolsonskoye. V. Kuznet-
. Tobolsk Province: Bere; zovsky distr., Bere-
Rozhdestvensky s.n. (LE): Tarsky distr.,
Rybinsk, near Pustynnoye, V. Varentsov s.n. (LE). Yakutsk
| ppc State: Yakutia, Suntarsky distr.. upper Vil-
| River, Tuoikhaia, by Chona River,

150/22 (LE).

lb. Paeonia anomala subsp. veitehii (Lynch) D.
Y. Hong & К. Y. Pan, Novon 11: 317. 2001.
Paeonia veitchit Lynch, Chron.

46: 2 tab. 1.

Gard.

J. Kildushewsky

ser. 3.

1909. TYPE: China. W. Sichuan:

Tatien-lu (Kangding), 8—10.000 ft.. E. H. Wil-
son (for James Veitch & Sons) 3034 (holotype.
K!, photo, PE!).
Аи = beresowskit ا ا‎ Bot. Mater. Gerb. Glavn.
Bot. Sada RSFSR 2: 15 Jan. 1921.
Lx shit (Komaroy) hipezinsk y.
SR 2: 46. 26 Mar.

Paeonia veit-
we var.
Mater. Gerb. 6 Gia). Bot. Sada RS
1921. China Oecid. a huan (Sichuan).

Sun-pan-tin (бо gpan). Guichua.” 9 June 1894. M
Be resowskii s.n. (lectotype, designated here. LE
seen).

Paeonia veitchii var. 5 = ex Cox) Stern, J.

aay Soc. 69: 1943. Paeonia ioodwardii

Stapf e Pl. Int md Farrer 43. 1930. TYPE:

1 Zone (Chuoni). K. Farrer 67 (holo-
type. E not seen).

Paeonia veitchii var. leioc arpa W. J. Wang & S. Н

FI. Reipubl. Mi ue Sin. PA 603. 1979. TYPE:
me Sichuan: Jinchuan. Kasa Township. Yin-
changgou, forests by stream, 2700 m. 26 Apr. 1958.

77248 Gel PE”.

. eile ‘chit var. uniflora К. Y.
pularis Sin, 27: 603.
Gaze, Xiongjiling. : 3000 m. mtn. summit.
June 1974. فا‎ Xizang Exped. Veget. Erin 034

PE!)

по!

Y

Roy.

^
~

1

‚ Wang,

Рап, FI. ‘publ. Po-

(holotype.

This subspecies, though distantly isolated from
Paeonia anomala subsp. anomala by the huge de-

serts of the Gobi, still very much resembles the

latter. The only remarkable difference between
them is the number of flowers on a stem. Paeonia

anomala subsp. veitchii usually possesses 2 to 4
blooming flowers in addition to up to 2 underde-
veloped flower buds. Very rarely only the terminal
flower blooms in addition to up to 3 flower buds.
Paeonia anomala subsp. anomala possesses only a
single terminal blooming flower, without or infre-
quently with 1 to 3 underdeveloped flower buds.
The subspecies is widely distributed in China:
southeastern and central Gansu, southern Ningxia,
the Qinling Range of Shaanxi,
and the eastern extreme

eastern Qinghai,
Shanxi, western Sichuan,
of Xizang (Tibet) (Fig. 3). Like subspecies anom-
ala, Paeonia anomala subsp. veitchii prefers rela-
tively moist habitats, growing in forests, grasses on
the edges of forests, bushes, or subalpine and al-
pine meadows with shrubs, at altitudes from 1800
to 3870 m.
Phenology.
April to early June, and fruits in August and Sep-

The subspecies flowers from late

tember.
Chromosomes. 2n = 10 (Hong et al., 1988).
Additional Tp, examined. CHINA. Gansu: Di-
ngxi, s. coll. s.n. (CPB). Hezheng: Xinzuang. Gansu Herbs
сар. s.n. (NWTC). E da Mt. Dalinke, Q. R. We
Ш . Jiangcha: E У à
Suet Kangle: Mt.
. Lianhua, M. S. Yan 17 55 (NWTC).

Kangxian: s. loco,

94

Annals of the
Missouri Botanical Garden

x PN
\ 0
¿NO Pd
N pt
‘S X
БА 2 60°
e hi m D MEE nm a
e
30° >
ө
130°
> ө ө 50°
e e
®
40° e e e
* e
е е
gon 222 227 *
* 72 40°
* * Tk * 4 *
Ру да. о
оо 120°
9069 о
50° OX? о
Соо О 30°
y о C2
со
8 O Oo?
la 6
~D O
60° 70° 80° 90° 100° 110°

Figure 3.
anomala; white circles: /

or several vouchers cited in the text.

5 coll. s. n. uera Lanzhou: M Xinlong, s. coll. 84

С Tiandu, s. 1 s.n. (NWTC). Linxia: near
y 834 (РЕ). Longdie: Dacaopo,
1. J. Zhou 708 w Мо: Lujing, Zhongchuan-
gou, J. Q. Wang 197 (NWTC); Mt. Luodadoujidela, J. P
Wang 15240 (PE); near Mawu, T. P. Wang 4594 (PE);
between Lintao and egi Ms dis nos 1689 e 7

Mt. Wutai, Taohe Exped. 3 3 (РЕ); Lamathan, K. S.
604 (PE). Taohe: J a 12829 (PE). Tsaluku to shi
men, J. E Rock er (PE). Tianshui: i Xinjia

Hsia 5707 (PE).“ : Anyuan, У. He 4316 (PE);
Zhucha, Y. Q. He 4915 (PE); ); Jinqiang үш. ip, Mt. Мао-
mao, Q. К. Wang 1869 NN). Xiahe: Chingshui, 7. P
Wang 6944 (PE); Tangarang. 1 О. К. Wang
7270 (NWTC). Yongdeng: Liane heng, Tulugou, J. L. Bai
8613 (NWTC). Yuzhong: Xinlong, near Venida aowan, s.
coll. s.n. (PE). Zhangxian: Сеш. distr., 1 s ^d.
03183 (PE); Mt. Guiqing, 1 od wre 4735 (PE);
Hediling, Mt. Kehu, Huanghe Exped. 4655 (P E Shi-
chuan Forest Farm, Jinhuacl thi, Lian, Wang et al. 79197
(NWTC). Zhouqu: Taozhou Forest Farm, Jiang & Jin
00386 (PE). a (Chuoni): Kache Forest Farm, Lian &
2o 31 (NW ©); Wanchang, Sangtanagou, Lian & Chen

pbi

=
—

—

=

S

©

=

2 Е.
O;
No
© f
— '
vu

=

—

Dongxia, Yu, Lu, Gu & Li 68 (PE); Mt. Laoye, Liang et

Distribution map of the Paeonia anomala species complex. Black c

"ircles: Paeonia anomala subsp.

Р. anomala subsp. veitchii; stars: P. intermedia. Each site in nis map is supported by a single

al. 378 (HNWP); Baoku, Z. H. Zhang et al. 4291
HNWP). Huangyuan: Mt. Banjie, P. C. Meg 8842 (PE).
5 Sanhei Forest Farm. Wang 1065
HNWP); 40 km W of Xining, S. А Zhen 0351 (PE).
Huzhu: ae Forest Farm, Guo & He 9012 (HNWP);
Qiaotou, Guo & Wang 6717 Р). Jainca: near Angla,
Liu & Luo 1040 (NWP) Pedi Maying 3 Ko-
ngjiazui, В. Z. Guo 6767 (HNWP). Golog: M
Farm, Hongjungou, W. Y. Wang 26818 (HNWP). Menyuan:
Semnyi, betw. Lihua & Dalong, Z. Y. Qing 1218 (HNW
PE); Semnyi, Zhugusi, Xielong. B. Z. Guo 7396 (HNWP):
Semnyi, Hankegou, Cans “Qinghai Exped. 2493 (PE).
Minhe: Gushan, Nanxia, I. H. Zhou 2528 (HNW P);
ien erbeishan, B. Z. Guo 7010 (HNWP). Tongren: Rong-

», В. Z. Guo 10232 (HNWP); Shuangfengxi, B. Z. Guo
10186 (HNWP). Xining [Sining]: Shangwuchuang, К. S.
Hao 779 (PE) Xunhua: Mengda Forest Farm, Guo &
Wang 25058 (HNWP); Il /

WP). Shaanxi: Huxiar
Phatinae. ig 2019 (PE). 1
longbei, W. J. Hsia 4539 (PE). М. Та
temple, W. Y. Hsia 4571 (PE); Sanchaixia, К. J. Fu 4441
PE): Dadian temple to oo temple, Hong & Zhu
PB85065 (PE). Shanxi: Seo ie
Wang & Tian 594 (PE). M
lage, Xiejiagou, Shanxi Exped. 684 (РЕ). Sichuan: Baox-
ing: Raozhi, Nibagou, Hong & Zhong PB82105 (PE):

p —

—

p

Volume 91, Number 1
2004

Hong & Pan 95

Paeonia anomala Complex

Е Zhonggan. МІ. 1 5 5

459-0246 (PE); Ganvanggou. I. T. () (PE); Dengch-
igou. 7. P Tu 4329 (PE): Lianghe a PM ele p
& Ren 5572 (PE). Barkam: near Puvajiao. A. Li 71029
(PE); near Kanzhugou. by river V. Li 70441 (PE):
Pwermagou. 209 Lumbering Ground. M. Li 70867 (PE):
Bwermagou, X. Li 70903 (PE): near Maan: Li 71645

(PE); Dalongjiaogou, X. Li 70685 (PE): near kafeiqiao. A.
Li 71196 (PE); Zonggag. X. Li 70719 (PE): Nazhugou. X.
Li 71087 (PE). Emei: Jieyindian, J. H. Tu 362 (PE). Dege
S. X. Jia 229 (PE). Garze: S bank of Yalongjia River, Y
W Cui 4348 (PE). Heishui: Shidiaolou Township. Sich-
uan-Econom. 459-1208 (PE): Sandougou, Sichnuan-Econ-
om. A59-1001 (PE). Jinchuan: Zosijia. E X. Li 10157
(P r4 Jiulong: Mt. Baitai, between Niupo & Baitai village.
s. Ying 3869 (PE). Kangding: Yulingong. Yingbapo. Hu
& He e (PE): Yulin Township. — Jiang &
5 (PE): Yulin ee 8 . C. Jiang
Taivangshan distr., Hu & He ve (PE):
Niugu village. W Sichuan Exped. oe et al. 243 (РЕ);

Xinduqiao. W Sichuan Exped. Kuan et al. 732 (PE):
Shade distr. M Along. Nanshui-Beidiao Exped. 02912
(PE): Zhonggu village. Dagaigou. W. Sichuan E n d. Kuan
et al. 352 (PE): between Kangding & Dawu. P C. Tsoong
5004 (PE). Lixian: Longxi. Yiduo village. Z. He 12559
(PE): Mivaluo. bo, yu, S. Jiang A-7162 (PE): Shuan-

Shu: anjingsi, 333 km milestone
of € eal highway. Zhang & Zhou 23742 (Pk):
Somang. 12 km milestone of Shuanjingsi— Багтай high-
. Shang & Zhou 22675 (PE). Ts
5021 (РЕ); 2 hor. by rive

jingsi. P X. Li 10100 (PE):

F. T. Wang 22930 (P "E . Mafang. Sichuan
Econom. (4-59) 2554 (РЕ); Зачем аһа. Sanlonggou, He
& {ма 1 I. d.

138 (PE). Mianning: Yejin Township. 5. E Zhu
; Huning distr., Jiexingou, S. Jiang 5708 (PE).
! Ун 6137 (PE). Qianning: S of town,
Jiang & Jin 2113 (PE); to Dawu, Zhang & Lang 57 (PE).
Sêrtar: 1 er S of Wuneda, S. Jiang 9082 (PE). Songpan:
m c S. Jiang A-7275 TE Mont. Occid. H. Smith
(PE). Tianquan: Mt. Erlong. Niaoniujingou. around
2 Hu & He 10088 (P E). we nec huan: Wolong Town-
D ru ed 459-2290 (PE): Wolong Nature
Zalang. 2 & fin Ph 85019 (PE). Xiao-
jin: Xihe VR Niuchanggou. Zha | Ren 6322 (PE):
Luobigou, bel N Zhang к qe 6082 (PE). Ya-
Mt. Ermin, Sichuan Plants Collection 0905 (РЕ);
Tanjiao to Malangeuo, J. S. Ying 3113 (PE). Zamtang:
e. right bank, S. Jiang 8930 (PE); ТО km №
of lbangmuda, S. Jiang 8965 5 (PE). Xizang (Tibet): Jomda:
Gamtog distr.. Qinghai-Nizang Exped. Vegetation Group
9893 (PE).

ship.
Resery YG;
jiang:

Lukesi Temple

Lede-

A. Meyer, in

1830. Paeonia anom-

Paeonia intermedia C.

Altaic 2: 277.

N

bour, Fl.

ala var. hybrida f. intermedia (C. Meyer)
Trautvetter. Enum. PI. Songor. 88. 1800.
Paeonia hybrida var. intermedia (C. A. Meyer)

1: 47. 19 Ol. Paeonia an-
. A. Meyer) Traut-
Tidi Imp. S. Pe-
1904. Paeonia
Meyer) O. &

Krylov. Fl. Altava
omala subsp. intermedia (C
Fedtschenko.

Sada 23: 351.
intermedia (C. A.
Beih. Bot. Centralbl.

in B.
Bot.
anomala var.

B. Fedtsch..

veller,
tersburg.

18: 216.

Ledebour

TYPE: the Altar Mountains,

(lectotype, designated here, K!).

1905.

Paeonia gon N. he 1zchoweli. Notul. Syst. Geogr. Inst.
Bot. l'iphlis. f asc. 21: 17. 1959. TY PE: Ge orgia.
ipo between Igoeti and Lamitskali, 16 May 195
TBI!

tschoweli s.n. (holotype. ).
Paeonta interme subsp. sig ceu * à Ovchinni-
ov. dH Tadzhikistanskot SSR. -10 & 531.

1975. nL Padzhikistan: dec cod ipii jugi
Hissarci ic. ad ripam m fl. Maichura. 5 km ab
ostio. 2500 m. 12.06.197 1. Glebowa 6 (holo-
pe. T AD not pre qd

The species has long been identified as Paeonta

anomala Т 197 d treated as a variety of P

1901). i
schenko, 1905: 1946:
subspecies of P. anomala (Trautvetter,

maulova,
Pan, 1979), a
1904). o
even as a form of P. anomala var. hybrida (Vraut-
vetter, 1860). These diverse and erroneous assign-
ments were made (1) the identity of P.
anomala, P. intermedia, and P. hybrida was not pre-
viously clear; (2) previous authors emphasized the

taxonomic value of indumentum on carpels; and (3)

Ps

because:

the characters of roots and calyces and their cor-
relation were not considered. Examination of the
types of the three taxa and extensive observations
on herbarium specimens and natural populations
Table 1)

independent species, distinctly differing from X

show that P. intermedia C. A. Meyer is an

—

anomala by its lateral roots tuberous to long-fusi-
form, sepals mostly (at least 2) rounded at apex but
not caudate. Also different from P. anomala, P. in-
termedia prefers relatively sunny and dry habitats.
Carpels vary from | to 5 in number. and from gla-
Ovchinnikov (1975)

properly treated the peony in Tadzhikistan as P

brous to densely tomentose.
intermedia, but his description of the new subspe-
cies pamiroalaica is unjustifiable. His description
and our extensive observations have not revealed
any significant difference.

This species is widely distributed in northern
Xinjiang. China (south to the Tienshan). Kazakhs-
tan, Kirghizia. Tadzhikistan, Uzbekistan.
Altai of Russia. One small isolated population was
found in Georgia (Hong & Zhou, 2003) (Fig. 3). Ht

meadows.

and the

grows in grassy and shrubby slopes.
steppes. or in sparse woods. at altitudes from 900
to 3250 m.
Phenology.
to late June and fruits from August to September.
10 (Hong et al..

—

This species flowers from late May
Chromosomes. 2n unpub-
lished).

Additional specimens examined. CHINA. "pr
Altai Mt.: Acad. Sinica Xinjiang Integr. Exped. 1065

Annals of the
Missouri Botanical Garden

(PE). Altay: Qiao’ati, G. L. Zhu et al. 6325 (PE): to Hal-
amaryi, Acad. Sinica 2917 M dos 10227 (PE); Klasu
Gou, R. C. Ching 2433 axiong Gou, Т Y. Chou
652100 (XJBI); " B D. Y. Hong et al. Popu-
lation No. 2 (PE); Xia = Gou, D. Y. Hong et al. Pop-
ulation No. 4 (PE). Bark dpi s. coll. 780 (XJBI).
Fuhai: Fuhai Forest Farm, C. L. Zhu 5665 (PE); № slopes,
T. Y. Chou et al. 652150 (PE. XJBI). Fukang: Tienci, Shi-
men, D. Y. Hong et al. 0190 (PE). Fuyun: Mica No. 3
Mine, /ntegr. Exped. s.n. (XJBI); Mica No. 4 Mine, /ntegr.
Exped. s.n. C . Habahe: Tielieke, Kelimu 10171
(XJBD; Wuzliti, Kelimu a JBI). Hoboksar: Songshu
Gou s. coll. 7385 31); Mt. Qiaganebo, /ntegr. Sh pi
10563 (PE, XJBI). Huoc e Aksu Commune, Y. R. Lin
74848 (PE); 5 Acad. Sinica Exped. 10402 (PE);
i, Yeguolin, W. Chang et al. 3316 (XJBD:
Xiaoxigou, А. К. N. Zhu 10414 (PE, XJBI). Mori:
Nangou, S. L. Chen 0040 (PE). Qapqal: 58 km e
to Zhaosu, Inst. Biology and А к 66 (XJBI). Она:
Biliuhe, J. С. Zhao 82-4288 U); Kuangou, Biology
81-8381574 (ХЈВІ); Tangf angen Forest Farm, /ntegr.

] ) iejin Commune, s. Q. Lin
34 (XJBI). Tacheng: Mt. “Bae rleike, N slope, /nteg.
Exped. 1200 (XJBI). Toli: Mt. Albakzin, е “т
К. C. Kuan 2611 (PE, XJBI). 5 = nsha ү.
Chou et al, 650392 (РЕ). Yining: Yinin est oe Tis
toulong valley, D. Y. Hong et al. Population. | & 092 (PE).
Yumin: уч Wild Bada Prunus Nature Reserve, J. C. Zhao
85-293 ‚ XJU). GEORGIA. Kartly: B. Lamis-
суры A ipei Hong & Zhou H99033 (PE). KAZAKHS-

Ili-Pri M ridges of Mt. Kirgizsky
Range, upper Su ata River, V. Golos-Kokov s.n. (LE); Is-
syk-Kul Province, Santash, iesu garden, in
& jus Wit s.n. (LE); Semirec 'hensk Province, N slop

—

>:
as
=
А
И,
j co
Сот

‚ (LE); SW Songorian д Mt. Emelsky
E); Taldy-Kurgan Province,
Mt. ius -Altyn- Emel pass to road
rkent, Grubov & Luboarsky 0 (LE); Zai-
liisky Alatau, Usun-Kargali River Valley, W Sukonnaya
Fabrika, Y. Goloskokov (1 E). E. Kazakhstan: Mt. Kalbin-
ok-tau, near oubinskle е А. Yunatov
| distr, Kusto
istr., near Kender-

Sary- Ozek-Dzha

& Borsowa 52 (L
sk Prov., Sonnet Alatau, S of Lepsinsk, R.

Rozhevits 55 (LE); W ridges of Songorian Alatau, Koksu
Gorge, near Koksuis V. Goloskokov (LE); Tarbagatai
Chenarak i маа & Buhaeva 298 (LE); Mt

eep gorge from the pass, Schipczinsky
5 Kazakhstan: Mt. Chatkalsky Range, Chat-
kal Valley, Mt. Piazak, O. Knorring 60 (LE); Prichuisky
кү, Sulunger Gorge, V. 5 0 ie 66 (LE

KIRGHIZ Dzhalalabad Province aE Kuren
distr., Mt. Range, S slopes, near AK-Terek, Le-
bedeva & Faleeva s.n. (LE); Kara- Alma, Toguz (Bulak), N
slopes, Jie einig s.n. ; Tianshan, Mt. d
Range, Mt. Elchin- Ustriuk, Kizilbulak Gorge, s. coll. s

E E) E rgana Province: Kirgizsky Alatau, Makbal
Gorge, Ty-Karyn River, б. /golkin 97 (L E); Oshsky distr.,
Ak-Bura valley, Mt. Kanida Pass, O. Knorring 25 (LE).

slope, A. Savenkova 29 (LE). RUSSIA. Altai: Alex Shrenk
s.n. (LE); Altai, Barnaul Province, between Kalmytskie

Музу & Mahanova, P. Krylov s.n. (LE). TADZHIKISTAN.

Gissarsky Mountain Range: Buhara, Gissar, Mtn. Zar
kamar Pass, V. Lipsky 1697 (LE). Darvazsky Mtn. lur.
N slopes, left bank of Zarako River, cai Havdak,
Shinova & Kinzikaeva 1550 (LE). Imam-Askari, Mt. W of
Darai-Imam, Bochantsev & Egorova 1014 (L " Peter I
Range, N slopes, Nazarak Valley, upper reaches, 15 km S
of Tadzhikabad, Ladygina, Ikonnikov & Fridman 1337
(LE). Vahshsky Mtn. Range, Mt. Hozreshi-Sho, above
Sary-Hosor, Sidorenko 185 (LE). Varzob Valley, right bank
of Maihur Gorge, NE slope, Stepanenko & С Кини
2514 1 E); Mountain pass between rivers Hava ts
E): upper Horanc hon, ad
ве 351 (LE). UZBEKISTAN. Tashkent Provine
Bolshoy Chimgan, Z. von Minkwitz 1190 (LE); Bolshoy
Chimgan, N stony slopes, V Bochantsev 547 (LE).

Literature Cited

Anderson, G. 1818. A monograph of the genus Paeonia.
rans. Linn. Soc. o 12(1): 248-283.

Dai, К. M & T. Н. Ying. 1990. A new species of the genus
Paeonia from Chins. Bull. Bot. Res. (Harbin) 1004): 33—

к” Candolle, A. P. 1818. ne Vegetabilis Systema Na-
urale 1: 386—394. Par
. 1824. P verme Systematis Naturalis Regni Ve-
getabilis 1: 56-66. Pa
Кейс 8 B. A. 19 "n p pop Tyan-shanya
3-105. Se Hort. Petrop. 23(2): 351—353.
1 0 A. P. 1961. Paeonia. Pp. 12— түз М. У. Рау-
ov ae Fiora of Kazakhstan, 4. Tab. 2. Alma-Ata.
Hong, D. Y. ‚ L. Zhou. 2003. Paeonia (Paeoniaceae)
in ЕА 'asus. Bot. J. Linn. Soc. 143: 135-150
‚ Z. X. Zhang & X. Y. Zhu. 1988. Studies on the
genus Paeonia (1)—Report of karyotypes of some wild
es in € p Acta Phytotax. Sin. 26(1): 33-34
. Y. Pan 1. 1994. fige, in Xinjiang,
China. Ас ta Phy Sin. 32(4): 349-355
‚ К. Y. Pan & N. J. Turland. 2001. (ner an-
omala Eu veitchii (Paeoniaceae), a new combination.
15-318

speci

L. 1802. Monographie Gattung Paeonia. En-
glers Bot. Jahrb. 14: 276
Krylov, P. 1901. Flora yid Altai 1: 47. Tomsk.
F. 1842. Flora Rossica 1: 74. Stuttgart.
. 1771. i enn Plantarum. 247. Holmiae.
Lynch, R. 1. 1890. А new classification of the genus
Марав J. y Hort. Soc. 12: 42
er, C. A. 1830. Paeonia. Pp. 276-279 in C. F. Led-
about (editor), Flora Altaica. Berolini

d 5 R. 1975. Flora Tadzhikistanskoi SSR 4: 6
0 & 531.

I edebour, C.

RUN P. s. 1789. Flora Rossica 1(2): 92-95, tab. 84-87.
St. Petersburg.

Pan, K. Y. 1979. Paeonia. Іп: W. T. Wang (editor), Flora
Reipublicae ee Sinicae 27: 37—59. Science
Press, Beijir

Schipe кзы . 1921. Synopsis of the E nus Paeonia.
Not. is en Hort. Bot. Petrop. 2(11-12): 41-47.
7. Paeonia. In: V. L. Komarov (editor), Flora

б; 35. Editio Akademii Scientiarum URSS

URSS 7
кии 1.

Schmitt, E. 1999, Les Pivoines. Étude systematique du
enre рар L. Plantes de Montagne 191: 574—583.

Stern, F. C. 1946. A Study of the Genus Paeonia. Royal
Horticultural Society, London.

Trautvetter, E. R. 1860. Enumeratio plantarum songori-

Volume 91, Number 1
2004

Hong & Pan
Paeonia anomala Complex

Alex Schrenk annis 1840-1843 collectar-
. 33: 87-88.
Fedtschenko (editor),

Petrop 23

carum, a Dr.
um. are Soc. Nat. Mose
904. ا‎ In: B.
Flora a the Tianshan TU Hort.

APPENDIX 1
INDEX TO ENSICCATAE EXAMINED

The figures in dde ses represent: la = Paeonia an-
omala sna ансат: 1b = Р реи subsp. veitchii:
2 = P interm

~
х

Acad. Sinica Bot. Inst. Exped. Xinjiang 1803 (РЕ.
XJBI) (2): Acad. Sinica Exped. 10402 (PE) (2): Acad. Sin-
ica Xinjiang Exped. 2496 (PE, XJBI) (la). 10227 (PE)

: Acad. Sinica Xinjiang deus Exped. 10657 (PE) (2):

es College 1051 (PE) Каа & Kashenko s.n.

(LE) (2): Alexandros, P. 17 zn (LE) ) (La). 219 (LE) (1а): Alex
Shrenk s.n. (LE)

Bai. J. L. 8613 (NW IC) (Ib): Beresowskii. M. (LE)
lb, type of Paeonia beresowskii Komarov); Biology Exped.

79250198 (XJBI) (2). 81 "8330478 (XIBI) (2): Boc dra am
V. 547 (LE) (2): Bochantsev € Egorova 1014 (LE) (2):
Borovikov. G. s.n. г ) (la): 1 el al. s.n. CS í Jal

Chang. 56 (XJBI) i
3316 (X]BD (2). "e (XJBI) A re
(ХЈВІ) (la): Chen & Ju s.n. (NW I 1b):
0040 (PE) (2); Cherepnin s.n. (LE) (la): С hing, К. СЕ
(PE) (la). А (PE) (2), gts (PE) (1а); А
652100 (XJBI) (2): Chou. et al. eee (PE) (2),
650868 (PE. XJBI) (2). EN 50 (PE. XJBD (2): Cui. N.
R. 091 (XJNU) (la), 86624 (XJNU) (la): Cui, Y. W. 4348

—

10255

1803

(PE) (1b). MN (PE) (1b).

Dolenko, G. 108 (LE) (la): Dranitsyn & Kochubei s.n.
(LE) (1a).

Ermolajeva, M. s.n. (LE) (1a); Evseeva, Z. 4406 (LE)
(la).

Fang, M. P. 4213 (LE) (la), 6037 (LE) (la); Farrer,
67 (E) (Ib. type of Paeonia O Stapf ex Cox):
Fedorov & Iljina 72 (L " (2). 128 (LE) (2); Fu. K. J. 4441

(PE) (1b); Fu. T. K. 834 (PE) ( na
, in. S. s.n. (LE) (la): Gansu Herbs
(NWTC) (Ib): Genina, S. s.n. (LE) (la): Gansu-Qinghai
Exped. 2493 (PE) (1b); Goloskokov. V. s.n. (LE) (2): Gon-
tscharow. N. 2051 (LE) (2): € a B. 512 (LE) (la):
»rigoriev & Buhaeva 298 (LE) (2): Grubov & Luboarsky
229 (LE) (2): Guo, В. 7. 5 E (HNWP) (1b). 7010
(HNWP) (Ib), 7396 (HNWP) (Ib). 10186 (HNWP) (1b),
10232 (HNWP) (1b): Guo & He 9012 (HNWP) (Ib); Guo
& Wang 6008 (HNWP) (Ib). 6717 (HNWP) (1b), 25058
(HNWP) (1b); Guo & Yang 9608 (HNWP) 08)
5 V. 515 (LE) (la): Hao. S. 770 (PE)
| (0. 4516 (PE) (Ib). 8 75 ir 19 He, 7
: He & Zhou 13338 (PE) (1b): Hong p
t al. Тоша 2 (РЕ) (2), pation 3 (PE) (la
E. | (PE) (2). deba ie 5 (PE) (la). Population
| (PE) (2). TER bein (P E (2 2); л 5 Zhong
PB82105 (PE) (1b): Hong D. : Zhu vA (PE)
(Ib). PB85040 (PE) 1155 ias (PE) (1b):
« He H95034 (А. CAS, K. MO, PE. L
Zhou H99033 (PE) (2):

Group s.n.

~

. 10463 РЕ) 11173 (РЕ) (1Ь);
Hiang, L uo & Time 7 (30 (PE)

о, G. 97 (LE) (2): dede & Fridman 892 (LE)

(1b).

) (La): Integr. Exped. 630 (XJBI) (1a).
10563 (РЕ. XJBI) (2).
Integr. Inst. Hydrol.

(2); Iljin. V. s.n. A
1200 (JBI) ( ). 7305 (XJBI) (la).
11829 (XJBI) s.n. (XJBI) (2):
Pedol & Biol. Res. 5788 (XJBD (2).
Jia, 5. E т (PE) (1b); Jiang & Jin 00386 (PE) (1b).
): Jiang & Xiong 34242 (PE) (1b). 34319
(PE ) (1b). Aid (PE) (1b): Jiang. S. 5768 (PE) (1b), 8874
. 8930 (PE) (Ib). m (PE) (1b). 9082 (PE 4 д
y ‚ A-7275 (PE) (1b); Jiang. X. C.
‚ 36433 (PE) (1b).
2}, _ 10369 (AJBD ( 2). 10614
(TBI) (2. type of Paeonia majko N.
shewsky. I. 150/22 (LE) (la); Kleme 175 E. 4d (L E
lla (LE) (la): ky pa B. 113 (LE) (
iced О. E) (2). 66 (LE) Ам
(LE) (1а); cia и S. 236 (LE) (1a); Котагоу, V. s.n.

(LE) (la): Korovkin, A. 290 (LE) (la): Krasnoborov. I.
6765 (LE) (la): Krishtofowich, A. s.n. a (LE) (1а); Krylov,
P. s.n. (LE) (2); Kuan, К. С. 2611 (PE. XJBD (2), 77309
(PE) (1b); Kuan et al. 243 En er (PE) (1b): Kuch-

erovskaya, S. 282 (LE) (1а); Kuminova & Alexeeva s.n.
(LE) (la); Kuvajev & Sabitov s.n. (LE) (La): Kuznetsov. I.
53 (LE) (1a). pe y (la). 103 (LE) (la) ШО
Kuznetsov, N. 199 (LE) (1a). 1991 (LE)

Ladygin 92 S (la), s.n. (LE) (2) Lg et al. 1337
(LE) (2); Lashinsky & 5 973 (LE) (1а): Lebed-
eva & Faleeva s.n. (LE) (2); Ledebour, s.n. (К)! 2. type 4

Paeonia intermedia C. ever); Li & Zhu. J.
10414 (PE, XJBD (2): Li 1 В а 10100 (P E) (1b), E
(PE) (1b). 10143 (PE) (1b): . 40247 (PE) (Ib). 70441

(PE) (Ib), 70510 (PE) (1b), pret (PE) (1b), 70719 (PE)
(Ib). 70867 (PE) (1b). 70903 (PE) (ТЬ). 71029 (PE) (1b).
71087 (PE) (1b), 71196 (PE) (1b). 71645 (PE) (1b), 74842

(PE) (1b), 74936 (PE) (1b). 77248 ( ) (Ib. type ol
Paeonia veitchii var. leiocarpa W. T. Wang & S. H. Wang):
Li 870147 (SHI) (Та). 87 е (SHI) (2): rie ho

72 (NWTC) (1b): Lian et al.
En Licent, P. 1

Chen 31 (NWT
(HNWP) (1b).

10) 1255
79179 (NWTC)

(Ib): Lin, S. Q. et al. 34 (XJBI) (2): Ling. Y. R. 1141 (PE)
(la, type of Paeonia pony nsts К. Y. Pan). 74243 (PE)
(2), 74848 (PE) (2). 74849 (PE) (2): Lic 1. 5659

Р a Dor de 6019 (PE) (1b). 61 78 (PE ) (1b):
Lips . 1697 (LE) (2): Liu & Luo 1040 (HNW P) Ih:
Liu & M 8308 (XJBI) (la): Liu. S. W. 2115 (HN y
(1b): Lomonosov a & Ivanova 89 (LE) (la); Long, X. F. é

PN

| 79 (LE) (la): Mao. Z. M. 10413 (XJBI) (la):
Mihno, P. s.n. (LE) (Ja): Minkwitz Z. von 1190 (LE) (2):
Morgan, P. 23 (К) (la).

ue Beidiao Exped. 02912 (PE) (1b).

Pharmac. Exped. 2019 (PE) (1b); Pobedimova 697 (LE)
(la) Pohle & Rozhdestvensky s.n. (LE) (1a): Polozhii x
Kandasova s.n. (LE) (la): Paniatovskaya s.n. (LE) (2
Price, М. Р. 293 (LE) (1а).

Qing, Z. Y. 1218 (HNWP. PE) (1b): Qinghai-Xizang Ex-
ped. Veget. س‎ 034 (PE) (1b. type of Paeonia кее
var. uniflora ‚ Pan), 9803 (PE) (1b): Qu. J. X.

(PE) (1b).

Reznic үе у. 49 ( LE) (la). 58 (LE) (la): Reznichen-
. 106 (LE) (1a). 360 (LE) (1а), s.n. (LE) (1а);
19 5 (P E ) (1b). 12829 (PE) (ТЬ). 13127 (PE)
(1b); Tode. I. s.n. (LE) (la): Rozhevits, R. 55
in. А. s.n. ) i

‚ (LINN) (la.

s.n.

(2): s. coll.

Schipezinsky 125

type of Paeonia бча А Lisa: Sede din: A.

98

Annals of the
Missouri Botanical Garden

(LE) (1а); S. Gansu Grassland Exped. 681 (NWTC) (1b):
бш. vit 684 (PE) (1b): Shanxi Exped. Wang & Tian
594 (PE) (Ib): Shinova & Kinzik aeva 1550 (LE) (2);
Shishkin, B. s.n. (LE) (2): * (LE
Shukin, S. s.n. (LE) (la); ichua an-Econom.
(PE) үе A59-1001 (PE) (1 b A59-1208 (PE) (1b), A59-

2554 (PE) (Ib), Sichuan-Econom. & Ya 838 (PE) (1b):
Sichuan Plants Collection 0905 (PE) (1b); Eis 185
(LE) (2); pid M s.n. (LE) (1a): 9 H. 2499 (PE)
(1b): Soe A V. 100 (PE) (1b); Sokolov, P. 13a um E) (1а);

Song, Z. P. 38544 en (1b). 39107 (PE) (1b); Stepanenko
& MM : 2514 (LE) (2); Suhareva, A. s.n. (LE) (1a).
Tang, T. 938 (PE) (1b); Teche Exped. 3243 (PE) (1b):

Tatarova & p oi 52 (LE) (2); Tolmatschew, I. 247 (LE)
(1а); Tomin, M. 67 x E) (la): 5 T. s.n. (LE) (2):
Troitsky, M. s.n. (LE) (1а); Tsoong. P. C. 5004 (PE) (1b).
5024 (PE) (1b), 8842 (PE) (1b); Tu, T. H. 362 (PE) (1b).
4329 (PE) (1b); Tugarinov, A. s.n. (LE) (1a); Turezaninow,
s.n. (LE) (1a)
Varentsov, V. s.n. (LE) (1a); Vereshagin, V. 296 (LE)
(la), 345 (LE) (1a); Ve rhovskaya & Mishin 104 (LE) (1a);
— E. 73 (LE) (1a); V vdrin, A. s.n. (LE) (1a).
Wang, F. T. 22930 (PE) (1b): Wang, J. Q. 197 (NWTC)
(1b); W ang, = R. 1869 (NW TC ) (1b). 7034 (NW TC) (1b),
7270 (NWTC) (lb); Wang. 1065 (
а ТОР. al (NWTC) (1а), 15240 (NWTC) (1а), 4594
WTC) (la), 6944 (PE) (1b); Wang, W. Y. 26771 (HNWP)
a 26818 (HNW a (1b), 27 060 (HNWP) (1b); Wang, W.

d et al. 27347 (HNWP) (1b); Wang & Zhou 19 (HNWP)

1b), 198 A (HNWP) (1b).

up Hie th Acad. Sinica 012 (XJBI (1a); Xu, L.
1. (PE)

=

pe D. 69 (LE) (la); Yan, M. S. 3 (NWTC)
(1b); Ying, J. S. 3113 CE) (1b), ان‎ ve) 0, 4582
(PE) (1b), As (PE) (1b); Ying, T. H. vs SHMU
(Та), 1001 (PE, SHMU) (Та), 1006 (PE, SHMU la), 1007
(SHMU, PE) (la, type of iuc altaica K. Mr "pt &
H. ving, 1008 (PE) (1а),

JO (PE) (1b), 6137 (PE) (1b); 1
A. 24 (LE) (2): Yurchenko, P. s.n. (LE) (la

Zapriagaev, F. 66 (LE) (2), 351 (I 7 = Zhang, Е M.
90-346 (XFNU) (la); Entes G. Z. 005 (HNWP) (1b);
Zhang & Lang 57 (PE) (1b); Zhang & gs 0502 (HNWP)
(1b); Zhang & Ren 5572 (PE) (1b), 6082 (PE) (1b), 6322
(PE) ) (1b); Zhang. 7. Н. et al. 0097 (HNWP) (1b), 0414
4291 (HNWP) (1b), 4317 (HNWP) (1b),
4320 (HNW P) (1b); Zhang & Zhou 22092 (PE) (1b),
22155 (PE) (1b), 22675 (PE) (1b), 23742 (PE) (1b): Zhao,
J. €. 82- 293 (PE, XJU) (2), ye К (РЕ, XJU) (2), s.n.
(PE, XJU) (2); Zhen, S. X. 0351 (PE) (1b); Zhou, H. J.
708 (NWTC) (lo Zhou, L. H. дз (HNWP) (1Ь); Zhu,
G. А 5665 (РЕ) (2), 5755 (PE) (la), 6345 (PE) (la).
80006 (NW m. 1b); Zhu, G. L. et al. 6325 (PE) (2). 6386
(PE) (2); Zhu, S. F. 20491 (PE) (1b).

PHYLOGENY OF
SMELOWSKIA AND RELATED
GENERA (BRASSICACEAE)
BASED ON NUCLEAR ITS
DNA AND CHLOROPLAST
trnL INTRON DNA
SEQUENCES!

Suzanne I. Warwick,”
Ihsan Al-Shehbaz.?
Connie А. Sauder,"
David F. Murray,” and
Klaus Mummenhoff"

ABSTRACT

sing sequence data from the ITS region (internal transeribed spacers ITS] а ITS2 of nuclear ribosomal DNA

and dhe 2.85 rRNA gene) and ns DN

A sequence data from the tral, intron, we

examined the evolutionary

re ема of and New World Smelowskta species with its putatively re nete genera (Brassicaceae). ITS and ті.

sequence dat e obtained from all 13 Sn

ielowskia species an

id from 13 taxa of the related genera Descurainia,

ae. Gorodlriu Hedinia, Polyctentiun, Redowskia, Sinosophiopsis, and Sophiopsis. Results Е maximum parsi-

mony analyses s g
plus Ermania. Corodko wia, Hedinia, Redowskta,
whereas the other clade included Smelowskia holmgrenii |
subelade). Descurainia formed a separate cla

Gorodkovia, and Redowskia,
not a spe C le = Were e xamine xd i In these ge ne ra)

genera Ermania.

rowed a polyphyletic origin for Smelowskia,

with the taxa spli t into two major clades. Smelowskia taxa

н тө and Sophiopsis formed one clade (Smelowskia s.l. clade),
(Holmgre ni sube lade) an id the genus Polyctenium (Polyctenium
le. ITS and trib molecular data, along with a comparison of key morpho-
logical traits for each genus, support recognition of a single genus that would include Smelowskia, th

e three monotypic

as well as the genera Hedinia, Sinosphiopsis, and Sophiopsis (although
. The molecular data are consistent v i

vith an Asian origin for Smelowskia

‚ followed by diversification in Asia Бай North America, subsequent to migration into arctic ык ын regions of

western North America. ITS sequence divergence estimates ranged from O to 4.1%

within Smelowskia s. str., and up

to 0.15% within the Smelowskia s.l. clade; whereas tral sequence divergence estimates ranged from 0 to 1.85% within
Smelowskia s. str., and up to 3.71% within the Smelowskta s.l. clade. indicating pleistocenic speciation within Sme-

lowskia as a whole.
Key words: Вт

Smelowskia, Sophiopsis. trnL..

rassicaceae, Descurainia, Ermania, Gorodkovia, Hedinia, IVS, Polyctenium, Redowskia. Sinosophiopsis,

The Brassicaceae are a large family of about 340
genera and over 3350 species distributed through-
out the world, primarily in temperate regions (Al-
Shehbaz, 1984: Appel & Al-Shehbaz, 2002). It is
a well-defined family easily distinguished from the
related Cleomaceae by floral and fruit morphology
(1.e.. cruciform corolla, tetradynamous stamens, and
septate capsular fruits (Hall et al., 2002).
classification of the family

Tribal
is. however, controver-
sial, and its phylogeny requires clarification (Koch,
2003; Koch et al., 2003). The characters tradition-
ally used at the tribal rank are few and include

orientation of the radicle in the embryo, number of

rows of seed in each locule, calyx orientation, tri-
chome type, fruit compression type (length-width
ratio), and features of the nectaries. Several tribal
systems have been proposed, and most of the tra-
ditional groupings, with the exception of the Bras-
siceae and perhaps the Heliophileae, are not mono-
phyletic (Koch et al., 2001. 2003: Appel &
Al-Shehbaz, 2002). Generic delimitation is also a
frequently encountered problem (Al-Shehbaz.
1984; Appel & Al-Shehbaz, 2002), and as many
other genera of the family, Smelowskia C. A. Mey.
is artificially delimited and lacks unique synapo-
morphies (Table 1). All species are perennials with

! We thank Herbert Hurka for providing
of the herbaria listed in Table 3. We

k

"D
Ottawa, Ontario КТА 0C6,

Mis

Canada. wat
P.O. Bos 2 9. St. T4
in Canada,

80 uri Botanic г I 71010
' Agriculture and ;
Ottawa, Ontario KIA ч

University of /

Eastern. С чеш

=
ш
em
Y
4
y
E
p
A
a
S
D
da
gs

TER Museum Drive,

^ De po of Botany,

Germa ni- Каша ck. DE

ANN. MISSOURI Bor.

lis, 1 63166-0299, U.S.A.
and Oilseed Research (

Fairbanks,
Fac ulty of Biology/Chemistry, University of Osnabriick, Barbarastr.

а sample of Hedinia tibetica. We are grate ful to the directors and curators
thank Victoria Hollowell for editorial advice.
e and Agri-Food Canada. Easter m TE and Oilseed Research Centre, Central Experimental Farm,

ihsan.al-shehbaz@mobol. org.
Centre, Central Experimental Farm,
Alaska 99775, U.S.A. ffdfm@uaf.edu.

11, D-49069 Osnabrück.

GARD. 91: 99-123. 2004.

Annals of the

100

Missouri Botanical Garden

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Volume 91, Number 1 Warwick et al. 101
Phylogeny of Smelowskia

Е 8 3 l- or 2-pinnatisect (rarely entire) leaves. ebracteate
E ef . = E
8, E - 5 = racemes, white, purple, or creamy white flowers.
is Do . me =
=| EL t z E distinct median nectaries, 6 to 30 ovules per ovary.
Su gu 5 8 =
AE 5 = 3 g variously shaped (linear, oblong, obovoid, ellipsoid,
2 = — T 2
3 or lanceolate) fruits, a prominent midvein on the
з Е. S 5 valves, entire stigmas, uniseriately arranged seeds,
= O E = L T u 3 "г uM . :
E: v5 2 T Б 8 and incumbent cotyledons. The majority of species
2 т c — * = » <= D ы J E |
Sle ae c Es СЕБЕ have soft, dendritic and forked hairs, herbaceous,
кро Ea .® 2— n = <€ E SE
cle s z Z È divided leaves soft in texture, and flattened or an-
- - — . кы
gled fruits. but S. holmgrenii does not have this
8 E
Б combination of characters.
ES . = С : А "AM
Е v E 5 Smelowskia has been variously delimited (taxo-
8 D = -à А HAE EN a
Si» . a T E S nomic treatments vary from 7 to 14 species). with
aj = E: = B : :
BIS 3 E E = several segregate genera placed in subtribe Des-
Als 8 5 Ba. © ——— —
curainiinae of the tribe Sisymbrieae (Drury & Rol-
_ Ф lins, 1952: Botschantzev. 1968; Velichkin. 1979:
2 y ^" = S Rollins. 1993; Czerepanov, 1995: Mulligan, 2001;
2/> 3 3 = = r ‘ Sy Е
31358 E E 2 = Zhou et al. 2001). As currently circumscribed,
бЭ | 7-9. m — 7 2 y
y 2% q = no : ПАШ ў ; à . ad
жр q E > E Smelowskia includes 13 species, of which 7 (5.
a am = oe TA m ae * . oe
A americana, S. borealis, S. holmgrenii, S. johnsonii.
a — S. media. S. ovalis, S. pyriformis) are North Amer-
Š E > 5 ай ican, 5 (S. alba, S. bifurcata, S. calycina, S. ino-
elu '* б = ee pinata, S. pectinata) are central and north Asian,
=|-= = EZ 3 т = j ens ;
"|? 8 = E vt and 1 (S. porsildii) occurs on both continents.
wi Ф o z om A = .
Names of accepted taxa, synonyms, and excluded
g E names in Smelowskia are listed in Table 2. Varieties
= v 2 = ‚= of S. calycina previously recognized in North Amer-
E © = © — і | \ g
«5 4 = mel — E um 3 4 . x
Sle та c E DN a ica are treated as distinct species.
gi 4 3 E б д ж
p р - = »- хе d: «== аар, : Р Р " А А
S |= S = > S Schulz (1924, 1936) placed Smelowskia in the
— Ф — = „= сч *
tribe Sisvmbrieae subtribe Descuraintinae. along
z ads with Descurainia Webb & Berth.. Hugueninia
E له‎ as E <3 6.3 = Rehb.. desa Cham. & Schltdl., Robeschia
= D 5.5 — S E і
Fie AE S5 E asia Hochst. ex О. E. Schulz. Sophiopsis O. E. Schulz.
rls gE ES 2 = == @ 0
= = © E 2. 3 and Trice о. O. E. Schulz. He divided Sme-
lowskia into section Prost tes (S. alba, S. caly-
x Ш . „ B . * . H я
_ LE cina, S. lineariloba. and S. ovalis) and section Po-
E v " T * 2 lyctenium (Greene) O. E. Schulz (S. fremontii). In
T = — ك‎ on. $ i А Р 4
Зо = = E 2 — North America. Rollins (1938) recognized Sme-
ROI = v = + E д : : Р 3 К м А
ЗЕ 3 E: © 3 lowskia (S. calycina and S. ovalis) and Polyctenium
Greene (P. fremontii) as closely related genera.
E Hultén (1945) placed the monotypic genera Me-
= v 2 3 5 lanidion Greene (M. boreale Greene) (Greene,
3 © К: — e
Elo «= F E E 1912) and Acroschizocarpus Gombóez (A. kolianus
SJE £ b 3 <=
Sle 6 E z © Gombócz) (Gombóez. 1940) in Ermania borealis
_ (Greene) Hultén. However, this transfer was inva-
з 2 | = lid. as the generic name Ermania (Chamisso, 1831)
“= a 6 < = = — Р . E
EE doses a was not validated until 1956 by Botschantzev (re-
7 E orf = 5 д = © . | | . : |
E Sjeo 28 8 88 8 5 zo viewed in Al-Shehbaz. 2001). Drury and Rollins
e [835 FsS 28 8 5 B ш и igiiur |
2 KE 3 a" ties 23” (1952) supported the congeneric status of Melani-
— = Ф 2 = д — | р . À
3 | dion and Acroschizocarpus and placed them in Sme-
ES "T Sa lowskia rather than Ermania Cham. ex Botsch., as
. = 2 — Sn 5
— ч S © ＋
© ye Es 38 8 SE S. borealis var. borealis and var. koliana, respec-
= 3 = — — DO : Р : Р
= £ Z oS 9 & №9 5 tively. Rechinger (1954) reduced his (Rechinger.
= — — р = 2278599 - "e : е.
D h 2 ә 5 1951) monotypic Chrysanthemopsis (C. koelzii

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Annals of the

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Volume 91, Number 1

Warwick et al. 103
1 ا‎ of Smelowskia

Rech. f.) to S. koelzit, which was later treated as a
synonym of S. calycina by Hedge (

[n a worldwide treatment of Smelowskia. Velich-
kin (1979) recognized seven Asian species (5. alba,
S. koelzii, S

tianschanica) and seven North

S. bifurcata, S. calycina, S. jurtzevii,

pectinata, and S.
American species (S. americana, S. lineariloba. S.
lobata, S. media, S. ovalis, S. porsildii. and S. spa-
thulatifolia). Rollins (1993) recognized five North
American species of Smelowskta. S. borealis (4 va-
S. calycina (4 varieties), S. holmgreni &.
Mulligan

rieties),
ovalis (2 varieties), and S. pyriformis.
(2001) recently recognized two additional species,
S. johnsonii (formerly S. borealis var. jordalii W. H.
Drury & Rollins) and S. media (formerly S. calycina
var. media W. H. Drury & Rollins). Mul-
ligan’s (2001) new combination of S. media is il-

Howey er.

legitimate because of its earlier use by Velichkin
(1979).

The purpose of the present study was twofold:
first. to test the monophyly of Smelowskia as delim-
ited by Drury and Rollins (1952), Botschantzey
(1968). Velichkin (1979), Rollins (1993). and Czer-
epanov (1995) (Table 2), with emphasis on North
American versus Asian taxa: second, to test the re-
lationship of Smelowskia with the North American
genus Polyctenium and putatively related genera.
Relationships to Smelowskia have been suggested
for Descurainia Webb & Berthel.. Redowskia.
Sophioposis by Schulz (1924. 1936). Ermania by
Drury and Rollins (1952), Hedinia Ostenf. by Ve-
lichkin (1979). and Sinosophiopsis Al-Shehbaz and
Gorodkovia Botsch. & Karav. by Al-Shehbaz (pers.
obs.). For comparative morphology of these nine

and

genera, see Table 1. Sequence comparisons of the
internal transcribed. spacers of nuclear ribosomal
DNA and the 5.88 rRNA gene (collectively. ITS
region) and the tral, intron region of the chloroplast
genome were used to assess evolutionary relation-
ships and taxonomic treatments of Smelowskta, ITS
sequence data are the most widely used nuclear
regions in phylogenetic analyses within families
(Baldwin et al.
ceae include Arabidopsis (DC.) Heynh. (O'Kane et
al. 1997: Koch et al., 1999a; Al-Shehbaz &
O' Kane, 2002; O Kane & Al-Shehbaz, 2003). Bras-
and other genera (Yang et al., 1999), Car-
damine L. (Franzke et al.. 1998). Caulanthus S.
Watson and Streptanthus Nutt. (Pepper & Norwood,
2001). (Koch et al., 1999b), Crambe
„ (Francisco-Ortega et al., 1999), Draba L. (Koch
& Al-Shehbaz. 2002), Halimolobus Tausch and re-
(Bailey et al., 200:
1999), Pachyphragma (DC.)

1995). Examples in the Brassica-

sica L.

Cochlearia 1.

N

Lepidium L.
Rchb.

lated genera
(Bowman et al.
and баата M. Král (Mummenhoff et al..

200la).

Sisymbrium L. (Warwick et al.. 2002).
(Koch & Mummenhoff, 2001). Vella L. (Crespo et
al.. 2000). and Yinshania Ma & Y. Z. Zhao (Koch
& Al-Shehbaz. 2000).
data also have potential phylogenetic utility for
(Sweeney & Price.

Thlaspi |

2

The trnlL intron sequence
Cardamine L. and Dentaria L.
2000). Cochlearia (Koch et al., 1990b),
and Cardaria (Mummenhoff et al.. 2001b).
Scop. (Bleeker et al.. 2002). and Sphaerocardamum
S. Schauer and related genera (Bailey & Doyle.
1999).

Lepidium
). Rorippa

MATERIALS AND METHODS

PLANT MATERIAL

Leaves (100 mg or less) were sampled from her-
barium specimens or silica-gel dried samples of
field-collected material (Table 3). Where possible,
multiple accessions were assessed for each species.
Ingroup species were selected based on available
material and to represent the morphological and
geographical diversity of Smelowskia and/or related

B
ge nera. ITS sequences (Table 3) were obtaine d from

laxa (13 species) of Smelowskia (05 accessions)
ad 13 species (23 accessions) from the purported
related genera Descurainia (D. californica (A. Gray)
O. E. Schulz. D. pinnata (Walter) Britton. D. sophia
(I.) Webb). Ermania (E.
Botsch.). Gorodkovia (G. jacutica Botsch. & Karav.).
Hedinia (H. tibetica (Thomson) Ostenf.). Polycten-
ium (P. fremontii (S. Watson) Greene and P. wil-
liamsiae Rollins). Redowskia (R. sophtifolia Cham.
& Schltdl.). Sinosophiopsis (S. bartholomewti Al-
Shehbaz). and Sophioposis (S. annua (Кирг) O. К.

Schulz, S. flavissima (Kar. & Kir.) O. E. Schulz. 5.
sisymbrioides (Regel & Herder) O. E. Schulz). The
tral, intron sequences (Table 3) were obtained for
13 species of Smelowskia (25 accessions) and 13

parryoides (Cham.)

species (17 accessions) from the above genera.
Five outgroup taxa were initially included in
both the ITS and tral
appropriate outgroup(s) was difficult, since with the
exception of the tribe Brassiceae, all other tribes in

analyses. Selection of an

the family are not believed to represent natural
groups. Representatives of two subtribes of Sisym-
brieae (sensu Schulz. 1936) included as
Arabidopsis thaliana (I Heynh.

were
outgroups, 1.€..
(Arabidopsidinae) and Sisymbrium irio L. (Sisym-
along with representatives of three other
(Arabideae). Brassica rapa

brinae),
tribes: Arabis alpina L.

(Brassiceae), and Capsella bursa-pastoris (L.)
Medik. (Lepidieae. Capsellinae). The ITS sequenc-
es of Arabidopsis thaliana. Arabis alpina, В. rapa.
C. bursa-pastoris, and S. irio and the trn, sequenc-
es of the first two were obtained from GenBank (Ta-

Annals of the

104

Missouri Botanical Garden

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Warwick et al.

Volume 91, Number 1

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Phylogeny of Smelowskia

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Volume 91, Number 1
2004

Warwick e 107

челин К Smelowskia

ble 3). Initial analyses showed that if the above five
species were included in the outgroup, the ingroup
was not monophyletic, as Arabidopsis (DC.) Heynh.
and Capsella Medik. formed part of the ingroup.
Subsequent analyses included these five taxa. with
Brassica, and Sisymbrium assigned to

only Arabis.

the outgroup.

DNA EXTRACTION

DNA was extracted from approximately LOO mg
or less of dried leaf tissue using Bio 101 FastDNA
Kit (Qbiogene Inc., Carlsbad, CA, U.S.A.) following
manufacturers. instructions. The final elution. was
performed in 80 wl of DES, and then brought to 10
mM Tris (8.0) by the addition of 1/10th volume of
100 mM Tris (pH 8.0).

DNA

ITS REGION OF NUCLEAR RIBOSOMAL

The entire ITS region (including internal tran-
scribed spacers ITS! and 1752 of nuclear ribosomal
DNA and the 5.85 rRNA gene) was amplifie «das a
single unit using primers 151-185 described i
O Kane et al. (1997) and I'TS4 described in W lius
et al. (1990). The amplifications were performed
using Ready-To-Go PCR Beads (Amersham Biosci-
ences, Piscataway, NJ. U.S.A.) and 2.0 pl of diluted
genomic DNA in a total of 25 pl.
were performed on a Thermolyne an ae ther-

Amplifications

mocycler (Techne Inc Princeton, NJ. Û ) using

an initial denaturing step of 95°C b 3 min.; 35
cycles of is 48°C for 35 sec., and
70°C for | min.: and a final extension at 72°C for
10 min. n СК reaction was run on a 1.0% TBE
NuSieve (Biowhittaker Molecular
Rockland, ME. U.S.A.) agarose gel followed by
band excision and purification using the GFN-PCR
DNA and Gel Band Purification Kit (Amersham
Biosciences).

Direct
primers (8-88 and ITS4) was performed by

for 35 sec.,

Applications,

sequencing using fluorescently labeled

Canadian Molecular Research Services (Ottawa,

ON, Canada) on a LICOR automated sequencer.
Base readings for both

forward and reverse se-

quences as well as an edited alignment for each
sample were verified with associated chromato-

grams. The ITS] and ITS2 sequences of accessions

3. 26. 37. 53. and 61 (Table 3) were obtained fol-
lowing the protocol given in Mummenhoff et al.
(1997

trni. INTRON

The trnl. intron was amplified using the e and d

primers described Taberlet et al. (1991). The

PCR Ready-To-Go PCR Beads
(Amersham Biosciences) and 0.2 pl of genomic

DNA in a total of 25.0 wl. Amplifications were per-

reactions used

formed on a Thermolyne amplitron thermocycler
Princeton, NJ. U.S.A.) using an initial

39 cycles of

(Techne Ine..
5 step of 94°C for 3 min:;
i 45 sec., and 72° for 45
sec.: and a final extension at 72° for 10 min. The
CR 1.0% TBE NuSieve
(Biowhittaker Molecular Applications) agarose gel
followed by purification with the GFX PCR DNA
and Gel Band Purification Kit (Amersham Biosci-

J for P min.. 50° for

reaction was run on a

ences).

Direct sequencing was carried out on a LICOR
automated sequencer using the DYEnamic Direct
ith 7-deaza-dGTP (Amer-

sham Biosciences) and with fluorescently labeled

eyele sequencing kit with

primers e and d. Both forward and reverse images
were captured and base-called with E-Seq (LiCor.
Lincoln, NE. U.S.A.) software. Forward and reverse
sequences for individual samples were aligned and
edited using AlignIR (Licor).
DATA SCORING AND ANALYSIS

The sequences were automatically assembled us-
ing the software ASSEMBLYLIGN (Kodak. New-
haven, CT. U.S.A.) and aligned using clustal in ME-
dui (DNA Star, Wl. USA.) and
further aligned by eve. For ITS, insertions/deletions
(indels), all of which appeared ITS] or
ITS2, were treated as missing data in accessions

Madison.

either

—

acking the sequence, with the exception of a 16
bp indel in IPS]. The latter indel formed part of a
19 bp region that was excluded from the analysis.
This approach retains phylogenetic information
from taxa not missing data at the indel. Boundaries
of the ITS] and ITS2 regions were determined by
comparison with the published sequences of Ara-
1997), Sisymbrium
(Francisco-Ortega et al.. 1999), and
2002). It has been

previously shown that indels in the tral. intron pro-

bidopsis thaliana (O'Kane et al.
altissimum L.
Sisymbrium irio (Warwick et al..

vide reliable phylogenetic resolution (Mummenhoff
et al., 2001b).
letions (indels) as missing data, and those indels of
2 bp and greater (10 indels in total) were treated

Therefore, we treated insertions/de-

as separate characters in the analysis and. scored
for presence/absence.

Maximum parsimony analyses of the aligned se-
quences of ITS and trnL were conducted separately
using the computer program PAUP*, version 4.0b2
Swofford, 1999). For the ITS

most parsimonious trees were generated using the

sequence data, the

—

heuristic search algorithm, which employed tree bi-

108

Annals of the
Missouri Botanical Garden

section-reconnection (TBR) branch-swapping.
equal weighted characters, with gaps treated as
missing data, with 25,000 random additions of the
sampled taxa, with 20 trees saved per replicate.
Limitations of computer memory required con-
straining maximum tree number at 40,000. A sec-
ond heuristic search was conducted using the 50%
majority-rule tree obtained in the above analysis as
the starting tree and the replicate allowed to swap
to completion using the TBR option. Statistics re-
lating to the amount of homoplasy in the trees, de-
scribed in PAUP*, were obtained for each tree and
a strict consensus tree was computed for each of
the two heuristic analyses. A third heuristic search
on the ITS sequence data was conducted where
Smelowskia was constrained to monophyly using
the constraints function in PAUP*, i.e., 2000 rep-
ТВК swap-
ping, and a maximum of 20 trees per replicate. Two
statistical tests available in PAUP*, the parametric
Kishino-Hasegawa and the nonparametric Temple-

licates with random addition of taxa.

ton. (Wilcoxon signed ranks) and winning-sites
tests, were used to evaluate the difference in length
between single most parsimonious trees from each
of the two analyses. For the trnL sequence data, the
most parsimonious trees were generated using the
heuristic search algorithm, which employed TBR
branch-swapping, equal weighted characters, with
gaps 2 bp or less treated as missing data and gaps
greater than 2 bp in length treated as separate char-
acters (scored presence/absence), with 10,000 ran-
dom additions of the sampled taxa, with 1000 trees
saved per replicate. In addition, a heuristic search
on the trnL sequence data was conducted where
Smelowskia was constrained to monophyly using
10,000 rep-
TBR swap-
ping, and a maximum of LOO trees per rep.

‘he ITS and trnL sequence data were combined

the constraints function in PAUP*, i.e..
licates with random addition of taxa.

for 47 accessions for which trnL data was available.
In order to test whether the data sets were congruent
and could be combined, heterogeneity among each
data set was assessed using the partition homoge-
neity test (Farris et al., 1995) as implemented
PAUP. No significant heterogeneity was detected (P
= 0.52), indicating that the two data sets could be
combined. The most parsimonious trees were gen-
erated using the heuristic search algorithm, which
employed TBR branch-swapping, with equal weight-
ed characters, with gaps treated as missing data for
ITS, and for trnL gaps 2 bp or less were treated as
missing data and gaps greater than 2 bp in length
treated as separate characters (scored presence/ab-
sence), with 25,000 random additions of the sampled
taxa, with 20 trees saved per replicate.

For the ITS, trnL, and combined ITS/trnL se-
quence data, 100, 500, and 500 bootstrap (Felsen-
stein, 1985) replicates, respectively, were generated
in PAUP* using a full heuristic search, with options
ACCTRAN, MULTREES = MULPARS, and TBR,
and each replicate generated with simple addition
sequence of taxa, in order to test the stability of
particular nodes in the parsimony analyses. Limi-
tations of computer memory required constraining
the maximum number of trees to 400 per replicate.
Pair-wise distance sequence divergence of ITS and
trnL were calculated for each accession pair in
PAUP* using the Kimura two parameter model (Ki-
mura, 1980) and the pair-wise deletion option for
gaps and ambiguous data.

RESULTS AND DISCUSSION
ITS SEQUENCE DATA

A total of 36 taxa (93 accessions) was included
in the analysis (Table 3), 5 of which were included
in the outgroup. The resulting multiple alignment
of the internal transcribed spacer (ITS) region, in-
cluding 5.85 gene, was 644 bp long. Sequences are
deposited in GenBank (accession numbers in Table
3), and the full alignment is available from the first
author. One region of ITS1 (19 bp) was difficult to
align and was excluded from the analyses (bases
109 to 127). For the remaining 625 characters, 389
base positions were constant and uninformative, 81
were variable but not parsimony informative, and

—

55 were potentially parsimony informative. The
ITS] and ITS2 regions exhibited similar amounts
of variation, with 129 variable in 260 sites (50%)
for ITS] and 99 variable in 201 sites (49%) for
ITS2. Only 8 of the 164 sites (5%) in the 5.85 gene
showed any variation.

The sequence alignment required the introduc-
tion of 13 indels in ITS] and 11 indels in ITS
Most indels were 1, 2, or 3 bp. However, a 7 bp
deletion in ITSI was detected in Brassica rapa, and
appears to be the same 10 bp deletion described
for its sister species B. oleracea L.
Ortega et al. (1999) A 16 bp deletion occurred in
the 19 bp ITSI region that was excluded from the

by Francisco-

analyses and is the same 16 bp deletion reported
for Sisymbrium altissimum by Francisco-Ortega et
al. (1999) and other Old World Sisymbrium taxa
(Warwick et al., 2002)

Among the ingroup taxa, the longest ITS region
(609 bp, excluding indels) occurred in Smelowskia
holmgrenii and the shortest (581 bp, excluding in-
dels) in Hedinia tibetica. The G + С content of taxa
within the ingroup was similar, with an average val-
ue of 55.9%.

—

Volume 91, Number 1
2004

Warwick et al. 109

Phylogeny of Smelowskia

Conspecific accessions of several species of Sme-
lowskia. Descurainia, Gorodkovia, and Polyctenium
had identical sequences over the entire length of
the ITS alignment: these are indicated in parenthe-
ses after the species name in Figures | and 2. Iden-

tical sequences were also detected for some Sme-

lowskia species (Fig. 2). For example. two
accessions of S. borealis var. koliana (acc. 28. 29)
had identical sequences to 5. media (acc. 4951).

ITS sequence divergence (excluding ambiguities)
among conspecific accessions was usually small:
Smelowskia alba (3 acc., range 0.17-0.34%). S.
americana (13 acc.. 0-0.85%). S. borealis var.
0—3.109€). S. borealis var.

bo-

realis (9 ace.. koliana

(Gombócz) W. H. Drury & Rollins (3 ace.. 0—
0.179€). S. calycina (6 acc., 0-3.23%). S. holm-
grenii (4 acc.. О-0.67%). S. inopinata (2 acc.. 0%),

0-0.17%). S. media (7 ace., 0—
0-0.84%). S. pyriformis
Descurainia e (2 acc., 0%),
5%). D. sophia (2 асс.
0%). Ermanta de j^ 0.33%).
kovia jacutica (З ace.. 0—0.509€), Hedinia tibetica
(2 ace., 1.39%), and Polyctenium fremontii (3 acc.,
0%).

The equal weight maximum parsimony analysis,

S. Johnsonit (3 acc..
0.67%). S. porsildii (6 ace.,
(4 acc., 0%),
D. pinnata (3 асс.

acc., Tue: =

which excluded autapomorphies. yielded 19,507
most parsimonious trees of 417 steps. with Arabi-
dopsis thaliana, Arabis alpina, Brassica rapa, Cap-
sella bursa-pastoris, and Sisymbrium irto as the out-
group taxa. When the 50% majority-rule tree of the
above 19,507 trees was used as the starting tree in
a subsequent heuristic search and then swapped to
completion, a total of 19.739 most parsimonious
trees was obtained. Homoplasy in the data set is
low as measured by a consistency index (CI) of 0.54
and retention index (RI) of 0.79. The strict consen-
sus tree from the two analyses was the same. Figure
39 most

parsimonious trees with bootstrap values, and Fig-

1 shows the strict consensus tree of the 19.7

ure 2 shows one of the most parsimonious trees with
branch lengths. Four major ingroup clades were ev-

ident: Smelowskia s.l. (Smelowskia s. str. and the
related genera Ermania, Gorodkovia, Hedinia, Re-
dowskia, Sinosophiopsis, and Sophiopsis). Holm-

grenii (Smelowskia holmgrenii). Polyctenium, and
Descurainia spp. Descurainia was clearly distinct
from the rest of the genera included in the ingroup.

trni INTRON SEQUENCE DATA

A total of 25 Smelowskia accessions and 17 ac-
cessions from related genera were included in the
analysis (Table 3), along with sequences from the
5 outgroup taxa. The resulting multiple alignment

of the Vn intron was 513 bp long. Sequences are
deposited in GenBank (accession numbers in Table
3). and the full alignment is available from the first
author. A total of 431 base positions were constant
and uninformative, 37 were variable but not par-
simony informative and 45 were potentially parsi-
mony informative. All Smelowskia accessions had a
trnl, intron length of 497 bp, with the exception of
S. holmgrenii (492 bp. deletion 371—375 bp). The
alignment required the introduction of 16 indels to
either related genera or outgroup taxa. Five were |
bp. | was a 2 bp indel. and 10 were greater than
2 bp. Two 7 bp deletions were observed in Sophiop-
sis flavissima (418—424 bp) and in Sinosophiopsis
bartholomewii (188-194 bp). А 9 bp
(392—100 bp) was observed for the 2
species, thus increasing trnL intron length to 506

—

insertion

Polyctentum

bp. the longest in the analysis. Á unique deletion
was observed for S. holmgrenii accessions (371—
375 bp). A unique 5 bp deletion (114—118 bp) and
a 59 bp deletion (229-288) were observed for Des-
curainia californica and D. pinnata. resulting in the
shortest trnL intron lengths in the ingroup (434 bp).
The latter deletion (plus 3 additional deletions of
193-228 bp. 289-370 bp. 376—383 bp) was also
observed in 3 of the 5 outgroup taxa (Arabis alpina.
Brassica rapa. and Sisymbrium irio). Brassica rapa
and Sisymbrium irio both had a 10 bp deletion
(121—130 bp). The 10 indels greater than 2

characters in the

bp were
treated as separate analysis.
bringing the total number of parsimony informative
characters to 55. The G + C content of taxa within
the ingroup was similar, with an average value of
: б.

The following 16 accessions had identical tral.
sequences: Smelowskia alba (ace. 1. as listed i
Table 3 and Figures). 5.
borealis var. borealis (acc. 20. 24).
32). S.

S. media (acc.

americana (acc. 4. 12).

S. calycina (acc.
inopinata (асс. 40), S. johnsonii (acc. 42).
48, 49, 51), S. pyriformis (acc. 62).
Ermania parryoides (acc. 73. 74). Gorodkovia ja-
cutia (acc. 77), Redowskia sophiifolia (acc. 84). The
two accessions (43 and 44) of S. johnsonii had iden-
tical sequences, as did accessions 71 and 72 of
Descurainia sophia.

e equal weight maximum parsimony analysis,
which excluded autapomorphies. vielded 20 most
parsimonious trees of 76 steps. with Arabidopsis
thaliana, Arabis alpina, Brassica гара. Capsella
bursa-pastoris, and Sisymbrium irio as the outgroup
taxa. Homoplasy in the data set is low as measured
by a СЇ value of 0.88 and an КІ value of 0.96.
Figure 3 shows the strict consensus tree of the 20
most parsimonious trees with bootstrap values, and

Figure 4 shows one of the most parsimonious trees

110 Annals of the
Missouri Botanical Garden

Clades

100 patie alba (1)

alba (3) Е

59 Smelowskia borealis var. koliana (27)
Smelowskia media (45-4
Smelowskia € bine koliana (28,29)
Smelowskia ame а (9
96 e elowskia americana d МА
smelowskia americana (1
smelowskia americana 4 8,10,11,14,16)

46)

Smelowskia americana

7

с
<
€
Smelowskia porsildii (56)

70 Smelowskia porsildii (61) A
Smelowskia porsildii (59 NA
Smelowskia porsildii "i 58,60) E
€

Smelowskia media )
Smelowskia borealis var borealis (2

82 |
| — Smelowskia borealis var. borealis (25
Smelowskia borealis var. borealis (2

те! ealis var. borealis

دں

N
N о

o
3
2
E
о
=
Ф
>
о
3
Ф
=
o
<
w
м
d
Ф
I
n
=
со
N
©

‹л
©
о
S
x
А
71
—
о

o Le is (62-65)
Smelowskia borealis var. borealis (21)
90 70 Smelo wskia johnsonii (42) Smelowskia s. l.
„
€

xmelowskia johnsonii (43,44) RS
xmelowskia calycina (30, 34,35)

100

59 Smelowskia bifurcata (1 7)
Smelowskia pectinata (55) A

7 ау
q |, Li: П íi (22)

7
Frmania narrunidias (73)
f J

Frmani. irl, (74 )

Smelowskia ovalis var. ovalis (52)
Hen s (53) NA

Smelowskia „ var. pis (54)
Smelowskia inopinata (40,41)
Gorodkovia jacutica (76,77)
— — 0 8 а (75)

Redowskia sophiifolia (84)
Hedinia tibetica (78)

100
94 — —— н Hedinia tibetica (79).

S Sophiopsis flavissima (87)
Sophiopsis annua (86

Sophiopsis sisymbrioides (88) AL
Ç

<

»melowskia holmgrenii (36)
3melowskia holmgrenii (37) Holmgrenii
NA

93 ко = A holmgrenii (39 )
P

Polyctenium

Capsella bursa-pastoris | Arabidopsis/
Arabidopsis thali | Capsella

Ag GT
,

100 89 Descurainia pinnata (68) Descurainia
Descurainia pinnata (69,70)

Descurainia sophia (71,72) m

Arahis alnina

Arabis alpina

Brassica rapa Outgroup
3

7
—

Figure l. Strict consensus tree of 19,739 most Parsimonious trees based on ITS sequences; tree length = 417
(excluding а ил characters), CI = 0.54, RI = 0.79. Bootstrap ба 's from 100 replicates appear
um bran: thes with 9t bootstrap support. Accession number as listed in Table 3

‘cles name; al Эйн ecific samples listed within parentheses had identical sequences.
лө skia s.l. Smelowskia and related genera Ermania, Gorodkovia, Hedinia, Redowskia, Sinosophiopsis, and
Sophiopsis|, 5 Holmgrenii, Descurainia) recognized in the analysis and the outgroup taxa are inc dicated to
the right. Asian (A) versus North American (NA) distributions are indicated in bold for species in the ingroup.

is give n in parenthes ses after
‘he four major clades

Volume 91, Number 1
2004

Warwick et
Phylogeny B Smelowskia

17

Si perm irio
Brassica rapa
Arabis alpina

5 changes

Figure 2.

One of the most vU Ra trees es based o
uninformative characters), CI = 0.41. zu

four major clades (Smelowskia s 1.

5 Smelowskia calycina (31) A
4, Smelowskia bifurcata (17)
melowskia pectinata (55) — —

—14 — Sap к ер!

Capse
z y a calorica (66. 67)

Descurainia у

Polyctenium. 5 mii. Descurainia) recognized ii

. Clades
7 Smelowskia alba (1)
18

>

media (45-48
ate realis var. koliana (28,29)
ma 9,50,51)

i (59
peus loweka porsildii (57. 58,60
1, Smelowskía calycina (30,34,35)
Smelowskia s.l.

n
o
=
`@
y
E^]
a

melowskia bore:
melowskia py е var erai (22)
/ var. borealis (18,

s (74)
wskia тора (40,41)
Smelowskia er var, nd
wskia ova vali

Gor
Redowskia sophiifol
He des иес 78)
a tibetica (79)
5 SIS аа (85)

ophi
1 Sophio ss p^ ymbriok les (88
Ame я sida reel (36) T
ee e hol nii (37) Holmgrenii
Smelowskia perii: (38)
1 Smelowskia -— (39)
if Polyctenium fremontii (80-82
Polyc eonim fi too (83)
bido, рыз thaliana

<=

Polyctenium
^ | Arabidopsis/
| Capsella

88
©

ella burs,

a (68
ani a pna (69,70)

=

Descurainia

Outgroup

1 ITS sequences: tree length = 417 (e cluding a

The aha of characters supporting each e lade i is indie ‘ated,

ı the analysis and the coe

taxa are indicated to the right. Asian (A) versus North American (N A) distributions are indicated in bold for species

in the ingroup.

with branch lengths. Four major ingroup clades

were evident: Smelowskia s.l. (Smelowskia S. Str.
and the related genera Ermania. Gorodkoria. Hed-

inia. Redowskia, Sinosophiopsis. and Sophtopsts).
Holmgrenii. Polyctenium. and Descurainia, In con-
trast to the ITS data, the trnl. data provided less
than 50% bootstrap support (Fig. 3) for the clade

containing the Holmerenii. Polyctentum and Ara-
Le] e 8

bidopsis/Capsella subclades (Fig. 4
I/ COMBINED SEQUENCE DATA

The combined II/, data set included 1143
characters: 830 were constant and uninformative.

112
and
The

which excluded autapomorphies. yielded 696 most

were variable but not parsimony informative,
201 were potentially parsimony informative.

equal weight maximum parsimony analysis.

parsimonious trees of 461 steps. with Arabidopsis

thaliana, Arabis alpina. Brassica rapa, Capsella
bursa-pastoris, and Sisymbrium irio as the outgroup
taxa. Homoplasy in the combined data set is low as
measured by a CI value of 0.60 and an RI value

of 0.8

the 896 most parsimonious trees with bootstrap val-

. Figure 5 shows the strict consensus tree of

ues, and Figure 6 shows one of the most parsimo-

nious trees with branch lengths. Analysis of the

112 Annals of the
Missouri Botanical Garden

Clades
p Smelowskia alba (1)
| Smelowskia inopinata (40)
Smelowskia calycina (32)
Smelowskia calycina (35) A
Smelowskia pectinata (55)
Smelowskia bifurcata (17)
es porsildii (56) A
Smelowskia porsildii (59) NA
Smelowskia borealis var. borealis (20,24)
Smelowskia borealis var. borealis (21) Smelowskia s. l.
Smelowskia borealis var. borealis (23)
i= Smelowskia media (48,49,51)
Smelowskia americana (4,12) NA
Smelowskia ovalis (52)
Smelowskia pyriformis (62)
Smelowskia johnsonii (42)
57 Bo cometa johnsonii (43)
Smelowskia johnsonii (44)
Ermania parryoides (73,74)
[— — Redowskia sophiifolia (84)
Gorodkovia jacutia (76)
Gorodkovia jacutia (77) A
Sinosophiopsis bartholomewii (85)
{ _—————— Hedinia tibetica (79)

100 B annua (86)

Sophiopsis sisymbrioides (88)
Sophiopsis flavissima (87)
Г вене pinnata (68)
C D inia californica (66)
Descurainia californica (67) Descurainia
95 74 y —Descurainia sophia (71)
E . LL Descurainia sophia (72)
99 po holmgrenii (36,38) - | Holmgrenii
Smelowskia holmgrenii (39) NA —

100 [^ Polyctenium fremontii (82) Polyctenium

Polyctenium williamsiae (83)
83 r— Arabidopsis thaliana Arabidopsis/
Capsella

96

1 Capsella bursa-pastoris
74 [— Sisymbrium irio

Brassica rapa Outgroup

Arabis alpina

Volume 91, Number 1
2004

Warwick et al. 113

19 of Smelowskia

combined data set yielded a topology that was near-
ly identical to that obtained from the analyses of
the ITS data set, with either the same or slightly
better bootstrap support. Four major ingroup clades
were evident: Smelowskia s.l. (Smelowskia s. str.
and the related genera Ermania, Gorodkovia, Hed-
inia, Redowskia,
(bootstrap support increased from 90 to 97%),
Holmgrenii (Smelowskia holmgrenii), Polyctenium,
As in the ITS analysis, 5.

holmgrenit was very distinct from the Smelowskia

—

Sinosophiopsis, and Sophiopsis

and Descurainia spp.

s.l. clade and formed the sister clade to Polycten-
ium, although bootstrap support was reduced to
15% compared to 93% for ITS data.

RELATIONSHIPS AND CIRCUMSCRIPTION OF SMELOWSKIA
l. SMELOWSKIA S. STR.

The ITS results indicate that 5melowskia sensu
Schulz (1924. 1936) is not a monophyletic genus.
Smelowskia species were split into two major
clades, with S. holmgrenii (designated the “Holm-
erenii” clade) forming a sister group to Polycten-
ium. The remaining Smelowskia taxa (Smelowskia
s. str.) were included in a single clade (Smelowskia
S. I.), along with other genera. The same pattern was
apparent for the trnL sequence data. When Sme-
lowskia was constrained to monophyly in separate
analyses of the ITS and trnL data, using the con-
straints function in PAUP* and subjected to the
same heuristic search as the unconstrained analy-
sis, most parsimonious tree length increased by 43
steps from 417 to 460 steps for the ITS data and
increased by 13 steps from 76 to 89 steps for the
irnL data. These trees were highly significantly dif-
ferent in length (P < 0. 0001) E on both the
parametric Kishino-Hasegawa test and the non-
parametric Templeton (Wilcoxon signed ranks) and
winning-sites test.

ле ITS- and trnb-based Smelowskia s. str. clade
included S. alba, S. americana, S. bifurcata, S. bo-
realis, S. calycina, S. johnsonii, S. inopinata, S. me-
dia, and S. pyriformis. With
the exclusion of S. holmgrenii, the general ITS-

S. ovalis, S. porsildii,

r. basi-

Rollins

based circumscription of Smelowskia s. st

cally follows Drury and Rollins (1952),

1993), and Velichkin (1979). The first two ac-

counts are essentially identical, but Velichkin rec-

ас

ognized additional North American species, all of
which were treated by the other two authors as va-
2). Velich-

kin depended extensively on the degree of devel-

rieties or synonyms of 5. calycina (Table
opment of nectar glands, abundance of simple
versus branched trichomes, and shape of the sep-
tum to distinguish most species. However, these
characters are so variable even sometimes within a
population, that it is highly doubtful if they have
any value in the separation of species and were,
therefore, justifiably ignored by Drury and Rollins
(1952).

Asian and North American species did not form
separate clades. Based on ITS data, the Asian Sme-
lowskia taxa were separated into three well-defined
clades, each supported by a 100% bootstrap value
(Fig.
occurred in 78% of the most parsimonious trees,
but had a bootstrap value of less than 50%, and is

1) and a fourth loosely supported clade (which

thus not shown in Fig. 1). The first clade included
three accessions of S. alba, the second two acces-
sions of 5. inopinata, and the third 5. calycina (4
The

fourth clade contained two accessions of 5. calycina

accessions), S. bifurcata, and S. pectinata.
and Ermania parryoides. Smelowskia pectinata and
S. bifurcata were sister taxa, separated by only two
steps. Morphologically they are also very similar,
differing primarily in leaf segment width, which 15
somewhat narrower in 5. pectinata than 5. bifurcata
(Velichkin, 1979). The molecular and morphologi-
cal data are consistent with the reduction of 5. pec-
tinata to synonymy of the earlier-published 5. bi-
furcata.

With respect to the North American taxa, three
species were monophyletic based on ITS data: Sme-
lowskia americana (supported by a 96% bootstrap
value), S. johnsonii (10% bootstrap value). and S
pyriformis (4 accessions with identical sequences "
Smelowskia porsildii, which is both North American
and Asian, also formed a single clade (70% boot-
strap value). The other North American taxa, 5. bo-
realis and S. media, were not monophyletic based
on ITS data, while relationships of the samples of
S. ovalis were not resolved by the ITS data

€

d 3.

e length = 76 (ex

cluding parsimony uninformative charac
x mee (400 trees per rep) appear above branches with = 500 bo
Ta

Strict consensus tree of 20 most parsimonious trees oe aa 2 analysis of the trnL intron sequences.
1 M

, Cl = RI = P .96. Bootstrap values from 500

El support. Accession number as listed in

3 is given in parentheses after the species name; all conspecific өзө. ч s liste " я тн had identical

sequences. The four major clades (Smelowskia s.l.,

Polyctenium,

Holmer analysis

i, Descurainia) recognized in the

and the outgroup taxa are indicated to the right. Asian (A) versus Noah а (NA) distributions are ibe in

bold for species in the ingroup.

114 Annals of the
Missouri Botanical Garden

____ Clades
| Smelowskia alba (1)
| Smelowskia inopinata (40)
¡Smelowskia calycina (32)
Smelowskia calycina (35)
“таша | Smelowskia pectinata (55)
Smelowskia bifurcata (17)
2 Smelowskia porsildii (56) NA
Smelowskia porsildii (59)
Smelowskia borealis var. borealis (20,24)
E | Smelowskia borealis var. borealis (21)
4 smelowskia borealis var. borealis (23)
Smelowskia media (48,49,51)
¡Smelowskia americana (4,12) NA
Smelowskia ovalis (52) Smelowskia 5.1.
Smelowskia pyriformis (62)
Smelowskia johnsonii (42)

N
=

Smelowskia johnsonii (43)
Smelowskia johnsonii (44)
Ermania parryoides (73,74)
Redowskia sophiifolia (84)
FGorodkovia jacutia (76)
Gorodkovia jacutia (77)
Sinosophiopsis bartholomewii (85)
Hedinia tibetica (79)

8 | Sophiopsis annua (86)
Sophiopsis sisymbrioides (88)

L2. Sophiopsis flavissima (87)
—5— Descurainia sophia (71,72)

B Descurainia pinnata (68) 3
+ е on Descurainia

E

N

Descurainia californica (66)
Descurainia californica (67)

— —

Smelowskia holmgrenii (36,38) NA

Holmgrenii

Arabidopsis thaliana Arabidopsis/
Capsella bursa-pastoris _ | Capsella
Polyctenium fremontii (82) NA

Polyctenium
Polyctenium williamsiae (83)

1 Sisymbrium irio
Brassica rapa Outgroup
— Arabis alpina =

Figure 4. One of the most parsimonious trees based on trnL sequence analysis. Tree length = 76 ои
parsimony uninformative characters), Cl = 0.88, RI = 0.96. The number of characters supporting each clade
indicated. The four major clades (Smelowskia s.l., Polyctenium, Holmgrenii, Descurainia) recognized in the an: as
and the outg group taxa are indicated to the right. Asian (A) versus North American (NA) distributions are indic ated in
bold for species in the ingroup.

Volume 91, Number 1 Warwick et al. 115
2004 1 of Smelowskia

Clades

Smelowskia alba 0)

Smelowskia media (51) NA

mel
ес calycina (35)
Smelowskia calycina (32
Smelowskia borealis var. borealis (20) |
Smelowskia johnsonii (42)
87 Smelowskia Johnsoni (43)
tien johnsonii (44) N
melowskia borealis var. borealis (21)
is wskia borealis var. borealis (23)
Smelowskia borealis var. borealis (24)
пев valis (52)

—

Smelowskia
|

66

= 5 (73)
— | 74)
Redow skia sophiifolia (84)
99 p— —— Gorodkovia jacutia (75)
UH 5 jacutia (77) A
[———— Sinosophiopsis bartholomewii (85)
9)

LL P tibetica

100 Sophiopsis annua (86)
F Sophiopsis кут Аа (88)
ا‎ e sima (87)

a (6

ә ninn.

523

100 Descurainia californica
100 100 Descurainia californica
ja sophia (71

) Descurainia

ph a
Smelowskia holmgrenii (36)
100 | Smelowskia holmgrenii (39) Holmgrenii
Fi ee Smelowskia holmgrenii (38) N
100 Polyctenium fremontii (82)
Polyctenium 1 E (83) =
B —— Arabidopsis thaliana Arabidopsis/
Ы———— Capsella a bursa- a Capsella
85 سم‎ a
L— ——— Brassic
Arabis Bana

Polyctenium

Outgroup

Figure 5. Strict consensus tree of 896 most parsimonious trees generated from analysis of the p ea ITS and
tral. intron sequences. Tree length = 461 (excluding parsimony uninformative characters), CI = RI = 0.81.
Bootstrap values des 500 replicates (400 trees per rep) appear above branches with > 50% үа support.

ecession number as listed in Table 3 is given in parentheses after the species name. The four major clades (Smelowskia
sl, Polyctenium. Holmgrenii, Descurainia) recognized in the analysis and the outgroup taxa are indicated to the right.
Asian (A) versus North American (NA) distributions are indicated in bold for species in the ingroup.

Smelowskia ovalis is morphologically a well-de- two accessions, resulting in a sequence divergence
fined species easily separated from the other spe- of 1.34%, ca. 10-fold greater than that observed
cies of the genus by having persistent sepals and between accessions of other Smelowskia taxa. Drury
ovoid fruits with a distinct style. The accessions and Rollins (1952) and Rollins (1993) recognized
corresponding to variety ovalis (ace. 52 and 53) had variety congesta on the basis of inflorescence shape
similar ITS sequences, separated by only three (.е., densely congested vs. more lax). silique length
steps, whereas variety congesta (acc. 54) was more (3-6 vs. 2-4 mm long), and trichome type (short
distinct and separated by seven steps from the other and branched vs. long and simple). In contrast to

116

Annals of the
Missouri Botanical Garden

Smelowskia alba (1)
Smelowskia media (49)
Smelowskia media (48)
Smelowskia media (51)
Smelowskia americana (12)
Smelowskia americana (4)

A

Smelowskia calycina (32)
Ermania parryoides (73)
Ermania parryoides (74) —

Smelowskia borealis var. borealis (20)
Smelowskia johnsonii (42)

Smelowskia johnsonii (43)

Smelowskia johnsonii (44

Hedinia tibetica

__Clades

|>

Smelowskia
s.l.

)
Smelowskia borealis var. borealis (21) N
Smelowskia borealis var. borealis NE
Smelowskia ovalis (52)
Smelowskia borealis var. н (24)
Smelowskia pyriformi
Smelowskia 1 (40)
Gorodkovia jacutia (75)
kovia jacutia (77)

)
Sophiopsis a

2

~

12 Sisymbrium irio
Brassica rapa
Arabis alpina

21

22

— 5 changes

Figure 6.
461 (excluding ка uninfor
clade is indica e four major clades (Smelowskia s.l.,
analysis and he Mes taxa are indicated to the right.
indicated in bold for species in the ingroup.

iative characters), CI =

the ITS data, which supports the recognition of the
two varieties, a critical re-examination of the type
material does not support these differences and,
therefore, we have proposed the reduction of this
variety to synonymy of S. ovalis (Table 2).

Based on ITS data, Smelowskia borealis was sep-
arated into six clades (Fig. 2). The first contained
S. borealis (acc. 27, 28, and 29), all corresponding
to variety koliana (Gombócz) W. H. Drury & Rollins

—.,

, Smelowskia holmgrenii (36)
! Smelowskia holmgrenii (39)
Smelowskia holmgre
18 Polyctenium fremontii (82)

, Polyctenium эмы аы (83)
La -— — Arabidopsis thaliana

le bursa-pastoris

ua (86)
` Sophiopsis pulling ie (88)
Sophiopsis flavissim ый
14 scurainia p ta (68)

7 | Descurainia iom (66)

escurainia californica (67)

Descurainia sophia
Descurainia sophia (72)

Descurainia

Holmgrenii

nii (38)
ри

Arabidopsis/
| Cap sella

alla

Outgroup

One of the most 5 trees based on combined E and trnL sequence analysis. Tree length —

0.60, RI = 0.81. The number of characters supporting each
Polyctenium, Holmgrenii, Descurainia) recognized in the

Asian (A) versus North American (NA) distributions are

and S. media (all accessions). The remaining S. bo-
realis accessions (var. borealis) formed loosely sup-
ported clades, except for the clade containing ac-
cessions 18, 20, and 22, which was supported by
a 94% bootstrap value. Smelowskia borealis is high-
ly variable, and some of the varieties (i.e., var.
dalii) recognized by Drury and Rollins (1952) merit
independent status (see S. johnsonii below). Both
S. borealis and S. media are diploid (Table 4), but

or-

Volume 91, Number 1
4

Warwick 117
19 a Smelowskia

Table 4. Chromosome numbers for Smelowskia, Ermania, Gorodkovia, and Redowskia taxa reported in the literature.
Taxon 2n Country of origin Reference

Smelowskia alba 12 Russia Zhukova & Petrovsky (1980)

S. alba 12 Russia Zhukova & Petrovsky (1984)

S. alba 12 eei : н (1972)

S. americana 22 е i AB) Packer (

S. americana 12 U.S O. UT, Drury & px Ж (1952)

S. bifurcata 12 s Krogulevich (1976)

S. borealis var. borealis! 12 USA. (AK) Murray & Kelso (1997)

S. borealis var. jordalii 12 U.S.A. (AK) Dawe & Murray (1979)

S. borealis var. koliana 12 U.S.A. (AK) Dawe & Murray (198 1a)

S. borealis var. villosa 12 U.S.A. (АК) Drury & Rollins (1952)

S. calycina var. calycina? 12 Russia Yurtsev € Zhukova (1972)
Zakharyeva & Astanova (1968)

S. calycina var. integrifolia 22 USA. (AK) Johnson & Packer (1968)

S. calyeina var. integrifolia 12 U.S.A. (АК) Murray & Kelso (1997)

S. media 12 U.S.A. (AK) Dawe € Murray (1981b)

S. porsildii* 22 U.S.A. (АК) Dawe & Murray (1979)

S. porsildii 22 U.S.A. (AK) Hollins (1993)

S. porsildii 32 Russia Zhukova & Petrovsky (1984)

S. porsildii 18 Russia Zhukova & Petrovsky (1984)

S. porsildit 24 Russia Yurtsev & Zhukova (1972)
Yurtsev et al. (1975)

S. pyriformis 12 U.S.A. (AK) Murray & Kelso (1997)

Ermania parryoides 12, 24 Russia Yurtsev & Zhukova (1972)
Zhukova & Petrovsky (1984)

E. parryoides 12 Russia Zhukova (1980)
Berkutendo et al. (1984

E. parryoides 24 Russia Zhukova & Petrovsky (1977. 1980)

Gorodkovia jacutica 12 Russia Yurtsev & Zhukova (1972)

z. Jacutica 36 Russia Yurtsev & Zhukova (1982)

Redowskia sophiifolia 20 Russia Yurtsev & Zhukova (1982)

! Reported as S. borealis.
? Reported as S. calycina

* Reported as S. calycina subsp. integrifolia var. porsildii

! Reported as S. calycina subsp. media Drury & Rollins.

they differ significantly in the morphology of their

caudices. flowers. and fruits. Smelowskia borealis
has simple and stout caudices, often branched flow-
ering stems. often purple sepals and/or petals, and
media has

angustiseptate fruits. By contrast. 5.

branched and slender caudices, simple flowering
stems, white or cream flowers, and terete or angled
fruits. Variety koliana, on the other hand, is quite
different in fruit morphology (oblong to spatulate
vs. obovate) and length (7-18 vs. 3-7(-8) mm long)
from variety borealis. and it may well deserve to be
recognized as a distinct species. Critical morpho-
logical. cytological, and molecular studies аге
needed to understand the phylogenetic relation-
ships within the S. borealis and S. media complex-
es:

Smelowskia johnsonii, recently described by
Mulligan (2001), would appear to be the same taxon

as S. borealis var. jordalii W. H. Drury & Rollins.

(Drury & Rollins) Hultén.

We have not examined the tvpe of the latter taxon.
but the original description is similar to the type
collection of S. johnsonii, except the latter. has
shorter fruits that are not spatulate. Smeloiwskia
johnsonii is morphologically very distinct from all
of the North American species and is easily distin-
guished by its densely white villous leaves, minute
styles (usually less than 0.5 mm long). caducous
calyx, and ellipsoid, slightly angustiseptate fruits.
The molecular data support the recognition of the
varieties of Smelowskia calycina (Drury & Rollins.
1952: Rollins, 1993, Table 2) as separate species
as in Velichkin (1979), with S

lycina, S. media, and S. porsildii each forming dis-

S. americana, 5S. ca-

tinct clades. Smelowskia calycina is strictly an

Asian taxon, and based on ITS data (Fig. 2) was

divided into two clades (ace. 30, ЗІ. 34. 35 and
32, 33). However. no obvious morphological differ-

ences were apparent between the herbarium spec-

118

Annals of the
Missouri Botanical Garden

imens in each clade. The ITS data for accession 35
support the inclusion of S. koelzii in S. calycina by
Botschantzev (1968) and Czerepanov (1995). The
North American S. media and S. porsildii are dis-
tinct cytologically (the former is diploid and the

atter is polyploid with various numbers; see Table
4). They also differ in their leaves and fruits. In S.
media the cauline leaves are divided and the fruits
are widest above the middle, whereas in S. porsildii
the cauline leaves are undivided and the fruits are
widest at the middle. The remaining North Ameri-
can varieties of S. calycina (var. americana (Regel
& Herder) W. H. Drury & Rollins and var. integri-
(Seeman) Rollins), as treated by Drury and
(1952). Rollins (1993), and Mulligan
(2001), should be recognized as S. americana, the
oldest name available at the specific rank. Velich-
kin (1974, 1979) recognized four distinct North
American species (5. americana, S. lineariloba, 5.
lobata, and S. spathulatifolia; see Table 2) in what
is treated here as 5. americana. However, Velich-
kin's delimitation of the last species included ma-
terial that belongs to S. porsildii. Further studies
are needed to elucidate whether or not S. spathu-
latifolia merits recognition.

2. SMELOWSKIA S.L. CLADE

Representatives of Ermania, Gorodkovia, Hedi-
nia, Redowskia, Sinosophiopsis, and Sophiopsis were
included within a well-supported clade along with
Smelowskia s. str., with bootstrap values of 90 and

1% based on ITS and trnl. sequence data, re-
spectively. Except for the three Sophiopsis species,
the degree of sequence divergence from Smelowskia
taxa for the other five genera fell within the range
observed among Smelowskia s. str. Each will be dis-
cussed separately below based on ITS and n di-
vergence from Smelowskia s. str.

Ermania Cham. ex. Botsch.

The ITS data fully supported the earlier taxo-
nomic transfer by Drury and Rollins (1952) of Er-
mania borealis to Smelowskia. These authors fur-
ther indicated (1952: 88) that "the type species of
Ermania, E. parryoides,
also be included in Smelowskia.”

might with some propriety
Although Polunin
(1959) transferred E. parryoides to Smelowskia, Er-
mania has been retained by most authors as a sep-
arate genus on the basis of having elongated lati-
septate siliques, i.e., strongly flattened parallel to
the septum. In the analysis of ITS sequence data,
H. parryoides formed a sister group to two acces-
sions of Smelowskia calycina in 78% of the maxi-
mally parsimonious trees (MPT) with a sequence

divergence of only 0.17-0.67%. Sequence diver-
gence from other Smelowskia taxa was also less
than 2.71%, supporting the taxonomic inclusion of
E. parryoides in Smelowskia. Data for the trnL in-
tron provided similar evidence for its inclusion in
Smelowskia, based on sequence divergence of 0—
1.01%. With the exception of accumbent versus in-
cumbent cotyledons, all its morphological features
can be accommodated in the current circumscrip-
tion of Smelowskia (Table 1). Ermania parryoides is
12,
24, as in other species of Smelowskia (Table 4).
Therefore, the morphological. cytological, and mo-

reported to have chromosome numbers of 2n —

lecular data clearly support Polunin's (1959) trans-
fer of E. parryoides to Smelowskia.

Gorodkovia Botsch. & Karar.

Both ITS and trnL sequence data indicate the
closeness of Gorodkovia to Smelowskia s. str. Based
on ITS data, sequence divergence between Gorod-
kovia and Asian Smelowskia taxa ranged from
1.51% to 3.40% and were only 0-1.22% based on
rn data. This monotypic genus, described in Bot-
schantzev and Karavaev (1959), is distributed in
eastern Siberia and the Russian Far East (Czere-
panov, 1995). With the exception of having biser-
iate instead of uniseriate seed arrangement, all oth-
er morphological features of G. jacutica fall within
the current delimitation of Smelowskia (Table 1).
Similar to the Old World Smelowskia taxa, it has a
12, 36. Morphologi-
cal, cytological, and molecular data do not support

chromosome number of 2n =

the maintenance of Gorodkovia as a genus distinct
from Smelowskia.

Redowskia Cham. & Schltdl.

Both ITS and trnL sequence data indicate the
closeness of the monotypic genus Redowskia to
Smelowskia s. str. Based on ITS sequence data,
sophiifolia was separated from the Asian taxa of
Smelowskia by a sequence divergence of only 2.02—

3.76% and 0-1.01% based on trnL data.
1 genus occurs in eastern Siberia (Czere—
panov, 1995). Schulz (1924, 1936) placed Redows-
kia and Smelowskia in subtribe Descurainiinae. Re-

This

dowskia differs from Smelowskia in fruit shape,
slightly 2-lobed versus entire stigmas, and а
versus uniseriate seed arrangement (Table 1).

also appears to have a distinct chromosome inch ar
of 2n = 20, as compared to 2n = 12, 18, 22, 24,
and 32 in species of Smelowskia (Table 4). Despite
these morphological and cytological differences,
ITS and trnL sequence data do not provide suffi-

Volume 91, Number 1
2004

Warwick et al. 119

Phylogeny of Smelowskia

cient support for the maintenance of Redowskia as

distinct from Smelowskia.

Hedinia Ostenf.

Both ITS and tral sequence data indicate the
closeness of Hedinia tibetica to Smelowskia S. str.
On the basis of IT
is separated from the Asian Smeloiwskia (5. alba,
calycina) by a sequence divergence of only 2.72—
3.95%. Hedinia.

contains four species, including one of Hedintopsts

S sequence data, Hedinia tibetica

a central Asian genus (Table 1).
Botsch. & Petrovsky recently reduced to synonymy
of Hedinia (Appel & Al-Shehbaz. 2002). Hedinia
tibetica was originally described under the illegiti-
mate name Hutchinsia (Thomson, 1852) and was
later transferred by Lipsky (1904) to Smelowskía.
Velichkin (1979) indicated that Smelowskia and
Hedinia ave closely related. Except for having brac-
teate instead of ebracteate racemes and lacking the

—

median nectar glands, there are no other characters
that clearly separate the two genera (Table 1). In
fact. as delimited by Czerepanov (1995), Hedinia
has species with bracteate and ebracteate racemes.
These two character differences are unreliable for
the separation of these two genera, as for most other
genera of (Al-Shehbaz. 2000, 2001).
Morphologic ‘al and us cular data support Lipsky’s

the family
transfer о tibetica, the generic type, to Sme-
lowskia. Comparative morphological and molecular
studies are required for H. altaica Pobed., H. czu-
kotica (Botsch. & V. V. Petrovsky) Jurtzev, Korob-
kov & Balandin, and H. mongolica (Kom.) Velich-

kin.

—

Sinosophiopsis Al-Shehbaz

Within the Smelowskia s.l clade from the ITS
analysis (Figs.
was the sister taxon to Hedinia tibetica, forming a

. 2). Sinosophiopsis bartholomewu

loosely supported clade (65% bootstrap value). It
was separated from Asian Smelowskia taxa by ca.
13 steps and a divergence of 2.54—
3.77%. Based on tral, data, it is separated by only

sequence
a steps and a sequence divergence of 0.82—
85%. It is one ol three species recently described
: this Chinese genus (Al-Shehbaz, 2000, 2002).
Sinosophiopsis differs from Smelowskia by the an-
nual growth habit and obscure midvein on the fruit

valves and differs from Hedinia in an even greater
number of morphological features (Table 1). Further

molecular studies on Sinosophiopsis furcata Al-
Shehbaz and S. heishuiensis (M. T. Wang) Al-Sheh-

baz. are needed to determine the distinctness of

Sinosophiopsis from Hedinia and Smelowskia.

Sophiopsis О, E. Schulz

Although included within the Smelowskia s.l.
clade, the three Sophiopsis taxa showed the greatest
divergence from Smelowskia s. str.. with a sequence
divergence of 4.65-6.45%. Based on both ITS
пі, sequence data, this central Asian genus of four
(Schulz, 1924: 1952). three
of which are included in this paper. was not mono-

and

species Botschantzev.

phyletic. Sophiopsis annua and S. sisymbrioides
formed a well-supported clade with a boots strap val-

100%

between them,

ue of and divergence of only
0.607%
separated by 35 steps and sequence divergence of

7.42% from the latter two species based on ITS

sequence
whereas S. flavissima was

data and by 11 steps and sequence divergence of
3.33%

differs from the other species of Sophiopsis by hav-

based on trnL data. Sophiopsis flavissima
ing stems with long, simple or forked trichomes in-
stead of dendritic ones, and perhaps merits inde-
pendent generic status. Schulz (1924, 1936) placed
Sophiopsis and Smelowskia in the subtribe Descu-
rainiinae, and Velichkin (1979) indicated that Sme-
lowskia was closely related to Sophiopsis. Morpho-

logical differences between the two genera аге
limited (Table 1). Schulz (1924, 1936) separated

Sophiopsis from Smelowskia solely on the basis of
seeds that become mucilaginous versus non-muci-

laginous, respectively, when wetted, a variable
character in many genera of Brassicaceae. Both
molecular data sets support the inclusion of So-

the

genus is not monophyletic and is the most distant

phiopis in the Smelowskia s.l. clade. However,

in the clade. Further study of the group, including
& Vved.,

is required in order to resolve its closest relatives

the fourth species, S. micrantha Botsch.
and lack of monophyly.

3. POLYCTENIUM GREENE AND SMELOWSKI/A
HOLMGRENII

The ITS
American Polyctenium (Polyctenium clade) as de-
limited by Rollins (1938, 1993), is monophyletic
and, together with Smelowskia holmgrenii (Holm-

sequence data indicate that the North

grenii clade), forms a well-supported clade (93%
bootstrap value) that is separated by 32 steps from
the Smelowskia s.l. clade. Arabidopsis thaliana and

y
—
>
*

Capsella bursa-pastoris, initially included in
phylogenetic analysis as outgroup species, were sis-
ter species to the Holmgrenii and Polyctentum
clades in a clade supported by a 91% bootstrap
value. Similarly for the trnL data, Polyctentum spp.
and S. holmgrenii were included in the same clade
(63% bootstrap value). along with A. thaliana and

C. bursa-pastoris and separated from the Smelows-

120

Annals of the
Missouri Botanical Garden

kia s.l. clade by nine steps. Although A. thaliana
and C. bursa-pastoris are members of different
tribes, several molecular studies (Galloway et al.,
1998; Koch et al., 2001) suggest these two taxa to
be more closely related than previously thought.
The unexpected position of these two genera in our
phylogenetic tree within the ingroup as sister to S.
holmgrenii and Polyctenium (subtribe Descuraini-
inae, tribe Sisymbrieae) underlines the profound
problems in tribal classification of the Brassica-
ceae. However, this is outside the scope of the cur-
rent study. Comprehensive molecular studies along
with critical re-evaluation of morphological char-
acters are needed to obtain a robust phylogenetic
framework that reflects a more natural classification
syslem.

Rollins (1938) separated Smelowskia from Polyc-
tenium by the petiolate, pliable leaves covered with
dense whitish tomentum, caudices covered by leaf
bases, petals differentiated into blade and claw, and
2 to 10 ovules per ovary. Polyctenium was said to
have non-petiolate, wity leaves, sparse, never whit-
ish pubescence, caudices free of leaf bases, petals
tapering from apex to base, and 12 to 28 ovules
per ovary. In his original description of S. holm-
grenii, Rollins (1950) expressed the difficulty in as-
signing this species to a genus. He placed it in
Smelowskia based on fruit morphology (terete, few-
seeded). He also indicated that it differed from the
other two North American Smelowskia, S. calycina
and 5. ovalis, by lacking the white dense tomentum
and by having entire, stiff, basal leaves. In addition
to their rigid, leathery leaves and almost exclusive-
ly simple and forked rigid trichomes, Polyctenium
species and S. holmgrenii also differ from Sme-
lowskia s.l. by having an obscure instead of prom-
inent midvein (Table 1). Smelowskia is essentially
an arctic-alpine genus with two areas of concentra-
tion, the Cascade and Rocky Mountains of western
North America and mountainous areas of central
and eastern Asia; Polyctenium inhabits semiarid ar-
eas at relatively low elevation in Nevada and ad-
jacent California, southeastern Oregon, and south-
егп Idaho, whereas S. holmgrenii is a narrow
endemic at middle elevations in Nevada (Rollins,
1950, 1993). Velichkin (1979) indicated that Sme-
lowskia, including S. holmgrenii, was closely relat-
ed to Polyctenium and Capsella, and the molecular
data herein do not contradict the association of
these genera. Morphological, geographical. and
both sets of molecular data, therefore, suggest evi-
dence that S. holmgrenii is more closely related to
Polyctenium thas to Smelowskia. The ITS and com-
bined ITS/trnL data were consistent with the inclu-
sion of 5. holmgrenii in Polyctenium; however, the

irnL sequence data provided limited support (boot-
strap value < 50%) for their placement in a single
clade, as shown in Figure 4. The inclusion of Ar-
abidopsis and Capsella in the same clade with these
taxa (Figs. 1, 2, 4-6), supports the treatment of $,
holmgrenii as a separate genus until further studies
are completed for this group of related taxa.

4. DESCURAINIA WEBB & BERTHEL.

Based on ITS sequence data, Descurainia formed
a well-supported clade (100% bootstrap value) that
was very distinct from Smelowskia, separated by 45
steps from both the Smelowkia s.l. clade and the
Polyctenium clade (Figs. 1, 2). Descurainia was di-
vided into two distinct clades for both ITS and trnL
data. The difference between the two clades was
particularly apparent for the trnL intron with D
californica and D. pinnata having two unique in-
dels, including a 5 bp (114-118 bp) and a 60 bp
deletion (229-288 bp) compared to D. sophia. Des-
curainia, a genus of about 40 species, is native to
many temperate parts of the world, with important
areas of diversity in both North and South America
(Rollins, 1993). It is clearly distinct from the rest
of the genera included in the ingroup. Morpholog-
ically, Descurainia is also very distinct from Sme-
lowskia by having glandular papillae, exclusively
dendritic trichomes, mostly yellow flowers, and
valves without a keel (Table 1). Schulz (1924, 1936)
placed both genera in the subtribe Descurainiinae,
and the molecular data suggest that Descurainia is
very distantly related to the Smelowskia s.l. clade.
Molecular data also indicate that D. sophia, the ge-
neric type, is distinct from the other two species,
and further phylogenetic studies are needed on the
genus.

In summary, both the ITS and trnL data indicat-
ed low levels of genetic differentiation among spe-
cies of Smelowskia s. str. (excluding S. holmgrenii),
in contrast to a wide geographic distribution (Veli-
chkin, 1979: map 169) covering central and north-
ern Asia and western North America. The molec-
ular-based clade also contained
Gorodkovia, Hedinia, Re-
and Sophiopsis, and thus
supports central Asia as the center of origin of Sme-
lowskia s. str., followed by diversification in Asia

Smelowskia s.l.
Ermania,

Asian taxa,

dowskia, Sinosophiopsis,

and North America, subsequent to migration into
arctic-alpine regions of western North America via
the former Bering land bridge as was suggested by
Rollins (1982). Such patterns were also suggested
for various disjunct Brassicaceae genera, among
them Stroganowia (K. Mummenhoff, unpublished
data) and Lepidium (Mummenhoff et al., 2001b).

Volume 91, Number 1
2004

Warwick et al.
Phylogeny of Smelowskia

121

ITS sequence divergence estimates, i.e., correct-
ed pair-wise distance values based on Kimura-2-
parameter model, ranged from 0 to 4.1% within
Smelowskia s. str., and up to 6.459€ within the Sme-
lowskia s.l. clade; whereas trnL sequence diver-
gence estimates ranged from О to 1.85% within
Smelowskia s. str., and up to 3.71% within the Sme-
lowskia s.l. clade. Recent calculations for several
Brassicaceae show that corrected ITS distance val-
ues (Kimura-2-parameter model) of 1% correspond
to ~ 0.5 to l million years (Koch & Al-Shehbaz.
2002. 2004).

within Smelowskia as a

indicating pleistocenic speciation

whole. Similar rapid radi-

ation and migration from Asia to Europe during the
Pleistocene was observed in Noccaea (Koch & AI-

Shehbaz, 2004) and Draba (Koch & Al-Shehbaz, in

prep.) and from Central Europe to Scandinavia and

the arctic region in Cochlearia (Koch et al., 1998,
999}

)).

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(Moscow & Leningrad) 62: 5-1223. [In Russian. |

— A — . 1980. E hne numbe rs and tax-
onomy of some species of the . Zhurn.
(Mosco ow & Leningrad) 65: i e 50, ln йө |

————, 1984. A po ps study of
some spec les pt the family sic
Asia. Bot. Zhurn. (Moscow & ое

[In Russian. |

cience vicis Beijing, and
ouis

iim hei rs of some

. Bot. Zhurn. (Moscow

usslan.

Press, St.

Chromosome

ı northern
230-240.

PHYLOGENETIC Pedro Torrecilla,?? José-Angel
RELATIONSHIPS OF VULPIA López-Rodríguez,? and Pilar Catalán?”
AND RELATED GENERA

(POEAE, POACEAE) BASED

ON ANALYSIS OF ITS AND

trnL-F SEQUENCES!

ABSTRACT

A phylogenetic study of Vulpia, fine-leaved Festuca (Festuca subg. Festuca p. p.), and other related genera of the
tribe Poeae (Poaceae) has been conducted using eta ва and combined analyses of DNA sequences from the
nuclear ITS region and the chloroplast trnL-F region. All five sections of Vulpia (sects. Vulpia, Monachne, Spirachne,
5 Apalochloa) and three sections and one 5 of fine-leaved Festuca (sects. Eskia, Festuca, Aulaxyper,
sect. Exaratae) were included in the analysis. Six minor annual genera that have been considered in the past to be
nét either to Vulpia or to these fescues (Psilurus, Ctenopsis, Cutandia, Narduroides, Micropyrum, Wangenheimia)
were also analyzed in order to estimate an evolutionary framework for this poorly known group of ephemeral or thin-
leaved grasses. Single representatives of other less related groups of Poeae (Festuca subg. Schedonorus and Drymanthele,
Lolium, Dactylis, Poa, Aaye Sesleria), Triticeae (Secale), ys Mr hypodieae (Brac hypodium) were also studied.
Phylogenetic analyses were performed based on parsimony and Bayesian inference criteria using Brachypodium dis-
tachyon as outgroup. “Our results cane ‘ate 1 7 Vulpia and the fine: eme Festuca are, respectively, polyphyletic and
paraphyletic assemblages of several taxa. A Жк lei пано group that encompasses the fine-leaved F
tuca and Vulpia lineages as well as he: he six ephemeral genera (FEVRE) has ek 1 from both the separate
and the Pe aie ITS and trnL-F analyses. Within this FEVRE clade Resa sect. Eskia is shown to be a paraphyletic
assemblage basal to the other taxa; the core of the FEVRE clade contains four supported ae representing, respec-
tively, the lineages Aulaxyper + Vulpia pro p (diplo id), Festuca /angenheimia, Psilurus /ulpia pro pm
(polyploid), and Spirachne + Monachne + Lore re сеа uae ав, constitutes a monospecific linea

with apparent but unsupported affinities to some a its potential closer relatives. Representatives of all the Vulpia
sections except those belonging to typical section Vulpia j join ina a paraphyletic бе supported assemblage that also
includes Cutandia, hom a plicata, and Ctenopsis. Two of the s ae annual genera, Micropyrum and Мий,
show distant evolutionary placements in the ITS and trnL-F em . The Festuca subsect. Exaratae taxa belong to a
phylogenetic lineage yas from those of the Festuca ovina Du Festuca) and F rubra (sect. Aulaxyper) fescues.
Nucleotide substitution rates show significant differences between most perennial and annual lineages; ки ed se-
lection is maintained in the slowly diverging ca groups, whereas the rapid adaptive evolutionary processes show
by the annual taxa may have pu in an increase ae rate in a. The Mediterranean region is a E
as the likely place of diver ergence of these grass lineag

words: Сіет opsis, Cutandia, Festuca, FEV RE gı group, ITS, Micropyrum, Narduroides, phylogeny, Psilurus, relative
rate test, trnL-F, Vulpia, Wangenheimia.

—
=

€
'

The genus Vulpia and other related genera of modern phylogenetic perspective. Single represen-
ephemeral grasses, mostly native to the Mediter- tatives of Vulpia have been included, however, in
ranean region, have never been investigated from a three recent phylogenetic studies of Festuca, a large

1 We thank Clive A. Stace, Jochen Müller, Robert Soreng, and Jerrold Davis for taxonomic comments and peer
revision of the manuscript, Clive A. Stace for 8. чы e of our materials and for providing us
seeds of some Vulpia taxa, David Posada and Fernando González-Candelas for their helpful аи оп Bayesian
analysis and Relative Rate Tests, Javier Fuertes, се Niet to- Feliner, and Ric ind G. Olmstead for critical review
of earlier versions of the manusc ript, Steve Russell for facilitating for us the design of the trnL F ‘fern” forward PNIS
Samuel Pyke for helping with the collection of some studied spec па. ii curatorial staff of the herbarium JACA for
sending us samples for DNA isolation, and the Conservation Council of the Andalusian Government for facilitating the
collection of fresh material and seeds of Festuca taxa at the Sierra три National Park. This work has been supported
by a Spanish Ministry of Education and Science grant (BOS2000- 0996 project), by a European LSF grant (NHM,
London) to PC, and by a Venezuelan CDCH doctorate fellowship to

Departamento de Agricultura, Universidad de Zaragoza, Miguel Servet 177, 50013 Zaragoza, España.

Present address: Cátedra de Botánica Sistemática, en Калый de Venezuela, Apdo. Postal 4579, 456323
Мане ‘ay, Estado de Aragua, Venezuela. [See footnote 2 for email address.
* Author for c orrespondence.

ANN. Missouni Bor. GARD. 91: 124-158. 2004.

Volume 91, Number 1
2004

Torrecilla et al.
Phylogenetic Relationships of Vulpia

genus of perennial species that contains important
forage grasses distributed on all five continents.

*

The pioneer work of Darbyshire and Marwie
(1992), based on analysis of chloroplast restriction
sites, first established the evolutionary links be-
tween Vulpia (V. myuros) and Festuca subg. Festu-
ca. Subsequent studies by Charmet et al. (1997)
and Torrecilla and Catalán (2002), based on anal-
yses of ribosomal DNA sequences, also confirmed
the close relationships between Vulpia (V. myuros
and V. fasciculata) and the fine-leaved fescues,
which include Festuca sects. Festuca, Aulaxyper,
and Eskia. These three mentioned works have dem-
onstrated that Festuca is a paraphyletic complex
and that Vulpia and Lolium fall within different
Festuca clades. However, whereas the phylogenetic
proximity of Lolium and Festuca subg. Schedonorus
(Schedonorus) has been ж EA in depth (Charmet
et al., 1997;
mation has been obtained eu respect to the re-

Саш et al., ‚ very little infor-
lationships between Vulpia and Festuca subg. Fes-
tuca

nad sampling of Festuca representatives was
included in the study by Torrecilla and Catalán
(2002) in which up to ten different lineages of the
genus Festuca were incorporated into the analysis.
These authors demonstrated that “Festuca s.l.” (in-
cluding Vulpia and Lolium) is monophyletic,
the

Festuca and the “fine-leaved” Fes-

yet
split into two diverging groups, so-called
“broad-leaved”
иса. Within this first group Lolium and Schedon-
orus formed a well-supported clade, whereas in the
second one Vulpia (V. fasciculata) was associated
with Festuca sect. Aulaxyper.

The taxonomic treatments of Vulpia, the fine-
leaved Festuca, and the six related annual genera
have varied over the last two centuries (Table 1).
Vulpia has been considered as a part of the genus
Festuca by some authors or as an independent ge-
nus by others. Linnaeus (1753) first described two
of the present species of Vulpia under Festuca, in-
cluding the type, Vulpia [= Festuca] myuros, and
Vulpia [= Festuca] bromoides. Gmelin (1805) sep-
arated Vulpia from Festuca based on its annual

abit, long-awned lemma, and very unequal
glumes. Hackel (1887) subordinated Vulpia as a
subgenus of Festuca. Although some later authors
still maintained Vulpia within Festuca, most con-
temporary agrostologists have considered Vulpia as
a genus on its own (Stace & Cotton, 1980; Clayton
& Renvoize, 1986). The circumscription of the ge-
nus Vulpia has changed depending on the inclusion
or exclusion of different genera, subgenera, or sec-
1981). The

Vulpia species differ in their breeding system, num-

tions within it (summarized in Stace,

ber and size of anthers, spikelet structure, number
of fertile/unfertile florets, and shape and size of the
lemma callus (Cotton & Stace, 1977; Stace, 1978a).
Vulpia sect. Loretia has been considered the most
similar group to Festuca as it includes robust an-
nuals as well as the three known perennial species
of Vulpia and shows strong chasmogamy syndromes
(Cotton & Stace, |
and Spirachne show intermediate traits between

Vulpia sects. Monachne
Vulpia sects. Loretia and Vulpia trending toward re-
duction in size and increasing self-fertility: these
groups encompass both chasmogamous and cleis-
togamous species, with sterile distal florets and
shorter anthers in the proximal fertile ones. Vulpia
sect. Vulpia has been interpreted as the most ad-
vanced group. as the majority of its taxa are strong-
ly cleistogamous species with single and small-an-
thered fertile florets. Section Apalochloa is a quite
distinct taxon: its only species (Vulpia unilateralis)
also shows a reduced habit and reproductive or-
gans, but its flowers are chasmogamous. Apalochloa
has been treated as an independent genus (= Nar-
durus (Bluff. Nees & Schauer) Rchb.) by several
authors (summarized in Stace, 1978a): however, as
most of its features are similar to Vulpia it has been
1978a: 198]

amended). Cotton and Stace (1976) found the chro-

classified within it (Stace, Stace,
mosome е number to be fixed within each Vulpia spe-
cies je 1) and to show a geographical distri-
bution pattern.

“Festuca sensu stricto” (subg. Festuca p.p.). as
circumscribed by Torrecilla and Catalan (2002), in-
cludes at least four distinct groups (as sects. Fes-
tuca, Aulaxyper, Eskia, and subsect. Exaratae),
though their evolutionary relationships have not
been conclusively established yet. These taxa are
characterized by their perennial habit and short-
awned lemma, traits in contrast to Vulpia, though
neither condition is free from homoplasy (Cotton &
Stace, 1977). Other taxa previously included in
Festuca by Hackel (1882) and Krivotulenko (1960)
(sects. Subbulbosae, Scariosae, and Pseudoscario-
sae) do not belong to this group as they are mem-
bers of the “broad-leaved” Festuca clade (Torrecilla
& Catalan, 2002).

Festuca sect. Festuca includes the type species
Е ovina (within a “Festuca ovina” complex). where-
as section Aulaxyper encompasses the red fescues
complex). Hackel (1882) classi-
fied these groups under one section Ovinae [= Fes-

(“Festuca rubra”

tuca] though separated into two different series by
the possession of exclusively intravaginal shoots
(sect. Festuca) versus extravaginal and intravaginal
ones (sect. Aulaxyper). Together sections Festuca
and Aulaxyper account for most species described

Annals of the

126

Botanical Garden

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ЭТШОПОХР |,

LH

Volume 91, Number 1
2004

Torrecilla et al.
Phylogenetic Relationships of Vulpia

in the genus. which are widespread in the Northern
Hemisphere. Section Festuca presents ploidy levels
from diploids to duodecaploids. though the high
polyploids are uncommon, most taxa having 2n. =
1х—бх;
though showing a similar diversity, is richer in taxa
6x and 8x (10x), and tetraploids and

2x and conversely, section Aulaxyper.

with 2n =
diploids are very rare (Ainscough et al., 1980).
Exaratae was described by Saint-Yves (1922) as
a subsection of section Ovinae (= Festuca) based
on the strongly invaginated leaf-sheaths shown by
1913). This Hackelian
Saint-Yves (1922) to sepa-
rate his subsection Exaratae from his typical sub-

these plants (Saint-Yves.
character was used by $

section Legitimae in Festuca (= sects. Festuca and
Torrecilla € Catalán, 2002). The Ex—
aratae group fescues are mostly local endemics
the
mountains. with ploidy levels 2n = 2x and 4x.

Aulaxyper: cf.

from Mediterranean basin and surrounding

Several annual genera of Poeae have been

grouped in а Vulpia—-Desmazerta com dex: Vulpia,
| I

Castellia.

Desmazeria.

Wangenheimia, Micropyrum,
Narduroides. Loliolum, Catapodium,
Cutandia. Vulpiella. Sclerochloa (Stace. 1981). Four

Ctenopsis. Wangenheimia. Micropyrum. and Cas-
g p:

Ctenopsis.

tellia) were characterized as close allies of Vulpia.
two others (Varduroides and Loliolum) as interme-
diate between Vulpia and Desmazeria, and the re-
mainder as more related to Desmazeria. Desmazer-
recently

ia, Catapodium, and Cutandia were

classified by Soreng and Davis (2000) as belonging

to their “Parapholiinae” subtribe. and Sclerochloa
as a member of their “Puccinellia complex." ac-
cording to their phylogenetic study of Pooideae
based on combined analysis of chloroplast restric-
tion sites and structural characters. None of those

groups were included in their “Loliinae” clade (=

Festucineae C. Presl.: sensu Tzvelev. 1982). where
Festuca is nested. Ctenopsis is similar to Vulpia in
several floral and leaf-blade traits (Paunero. 1963):
it has been treated as a section of the latter (Clayton
& Renvoize, 1986) though it differs in inflorescence
type and hilum length. Crenopsis has been consid-
ered to be close to but separated from Vulpia (Cot-
ton & Stace, 1977). Cutandia has also been clas-
sified as an independent rather different genus from
Vulpia (Stace, 1978b). Narduroides. Wangenheimia,
and Micropyrum were once included in the hetero-
geneous genus Nardurus s. (= Apalochloa p.p.:
Stace, 1978a) based on their annual habit and spi-
cate to racemose inflorescence. However. these
three show enough distinct morphological traits to
merit generic status (Stace, 1978a). Clayton and
Renvoize (1986) even included Narduroides in the

separate tribe Hainardieae Greuter. The latter au-

thors considered that Psilurus, a monotypic isolated
Mediterranean genus, was close to Vulpia.

Vulpia. Ctenopsis, Micropyrum, Narduroides, and
Cutandia have been classified as members of the
genus Festuca by different authors (summarized in
Stace, 1981).
been considered close to Vulpia (Stace. 19
Likely these predominantly diploid lineages radi-
ated in the Mediterranean area, the region in which

Wangenheimia and Psilurus have

they are endemic. A second divergence of polyploid
Northern-Hemisphere Festuca rubra and F ovina
taxa from more ancestral Mediterranean fine-leaved
diploids is also considered likely (Kerguélen &.
Plonka. 1989; Dubcovsky & Martinez. 1992).

In order to test these evolutionary scenarios we
studied representatives of the five recognized sec-
tions of Vulpia, of four sections and subsections of
fine-leaved Festuca, and of the small genera Psi-
Cutandia, Narduroides, Micropy-

lurus, Ctenopsis.

гит. and Wangenheimia (see Table 2). Phylogenetic
reconstructions are based on both independent and
simultaneous analyses of DNA sequences from the
nuclear ribosomal region (ITS1-5.8S-ITS2) and
from the chloroplast trnL-F region. eu in-
tron—irn-Leu 3’ exon—trnL-F spacer). The ITS re-
gion has proved useful for resolving the phylogeny
of Festuca and its allies (Charmet et al.. 1997; Саш
2000; Torrecilla & Catalan, 2002) due to
concerted evolution (Baldwin et al., 1995) and

rate of mutation (Torrecilla & Catalán.

et al.,

moderate

2002). The chloroplast trnL-F region has demon-
strated its phylogenetic value in other Poeae groups

(Brvsting et al., 2000).

the two different genomic data sources is intended

The combined analysis of

to obtain a consensus phylogeny and to interpret
1

the potential incongruences that might appear i
the separate nuclear and chloroplast: phylogenetic
reconstructions. a subject of importance to resolve
the phylogeny of this group of grasses where retic-
ulation has played a major role in speciation.
Rates of evolution differ significantly between
lineages of fast-to-slow aes ing ar (Bous-
1992: Gaut et al., 1992, 1996; Barra-
clough et al... 1996: ا‎ & ш:
2001). This phenomenon is particularly evident for

quet et al.

the grasses. which include some of the most rapidly

evolving within the monocotyledons
(Gaut et al..

grass species that propagale

sequences
1992). Annual or short-lived perennial
rapidly are expected
to show higher genomic variability than their re-
spective long-lived perennial congeners, suggesting
a release from stabilized selection (Саш et al.,
1997). Different substitution rates derived from di-

verse generation limes or alternative. reproductive

levi

strategies could. affect the reconstruc tion of phylo-

Annals of the

128

Botanical Garden

issouri

M

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129

Torrecilla et al.

Volume 91, Number 1

2004

Phylogenetic Relationships of Vulpia

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Torrecilla et al.

Volume 91, Number 1

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Phylogenetic Relationships of Vulpia

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Volume 91, Number 1
2004

Torrecilla et al.
Phylogenetic Relationships of Vulpia

133

genetic relationships via long-branch-attraction
and/or increased levels of homoplasy (Bousquet et
al.. 1992: Gaut et al., 1992, 1996, 1997). Because
Vulpia, the fine-leaved Festuca and the related
ephemerals constitute a case study with much di-
versity of annual and perennial grass lineages, we
have conducted relative rate tests of nucleotide
substitutions to clarify the selection of adaptive pat-
terns that may have impacted each different lineage
(Саш et al., 1997).

MATERIALS AND METHODS
TAXA SAMPLED AND SEQUENCE DATA

Sampling of representatives of Vulpia, the six re-

—

ated annual genera, and the fine-leaved Festuca
was accomplished by collecting fresh leaves and
herbarium vouchers. A total of 57 samples corre-
sponding to 52 taxa were incorporated into this
study. Morphologically variable taxa were se-
quenced two (Vulpia muralis, V. fasciculata, V. un-
ilateralis. H rubra) or three times (V. ciliata). Eigh-
teen of these samples that were previously included
in the ITS study of Torrecilla and Catalán (2002)
were sequenced for the trnL-F. region and used to
complete the sampling of the studied species. One
Vulpia myuros ITS sequence deposited by Charmet
et al. (1997) in Genbank was incorporated into the
study. The full list of taxa with indications of
names, authorities, localities, herbarium vouchers,
Genbank accession numbers, and ploidy levels is
presented in Table 2.

The sampling spectrum covered representatives
from the five recognized sections of Vulpia (18 sam-
ples). the fine-leaved Festuca (24), Micropyrum (2).
and one sample each from Ctenopsis, Wangenhet-
mia, Psilurus. Narduroides, and Cutandia. Three
representatives of the “broad-leaved” fescues, Fes-
tuca pratensis (Festuca subg. Schedonorus). F. altis-
sima (Festuca subg. Drymanthele). and Lolium per-
enne (Lolium), and one representative each from
Dactylis. Poa, Puccinellia, Sesleria (Poeae), Secale
(Triticeae), and Brachypodium (Brachypodieae)
were also studied (Table 2).

DNA isolation followed the same procedures
stated in Torrecilla and Catalan (2002) implement-
ed in some cases with the help of the DNAeasy
Plant Mini Kit (QIAGEN). Amplification of the ri-
bosomal ITS region (ITS1-5.88-ITS2) and further
sequencing were performed as indicated in Torre-
cilla and. Catalán (2002) using in both cases the
external primers KRC (forward) and ITS4 (reverse).
PCR amplification and sequencing of the trnL-F
region was conducted using either the external pair
primers "c" and “Г” (Taberlet et al.. 1991). or the

combined pair "fern" (forward primer: 5'-GGCA-
GCCCCCARATTCAGGGRAACC-3). (S. Russell.

pers. comm.) and "f" (reverse). 50 pl reactions

were prepared with 5 pl 10X buffer, 3 pl MgCl,
(50 mM). 4 pl dNTP (10 mM). 1 pl primer 1 (20
uM). I pl primer 2 (20 pM), 34.7 ul ddH,O, 0.5
pl Taq (1.5 units), and 1 pl DNA; the reaction

mixtures were subjected to one denaturing cycle of

—

min. at 94°C, 35 cycles of a 15 sec. denaturing
step at 94°C, 30 sec. annealing step at 45°C, and
l min. elongation step at 72°С, plus one 7 min.
72°C. The amplified products
were purified using the QIAgel extraction kit (QIA-
GEN). Purified products were then sequenced with
the ABI PRISM Dye Terminator Cycle Sequencing

Ready reaction kit (Perkin Elmer) and electropho-

termination cycle al

resed in an ABI Prism 377 automated sequencer.

The direct and reverse sequences of each sample
were compared and corrected using the program
Chromas. obtaining the respective consensus se-
quences. All chloroplast trnL-F samples and most
ITS rendered a unique sequence; however, some
polymorphic positions were detected in a few ITS
samples. Those sites were coded as polymorphisms
using the ambiguity IUPAC symbols. A total of 38
new ITS sequences and 57 new trnL-F sequences
of Festuca, Vulpia, Wangenheimia, Ctenopsis, Mi-
cropyrum, Narduroides, Psilurus, Cutandia, Lolium,
Dactylis, Poa, Puccinellia, Sesleria, Secale, and
Brachypodium have been deposited in GenBank
(Table 2). All but 1 (Festuca indigesta subsp. in-
digesta) of the 52 taxa studied have been se-
quenced for both the ITS and the trnL-F region. А
partial sequence of the ITS region of Festuca ner-
adensis (ЇТ®1 spacer, 5.85 gene) was included in
the analysis.

Each separate set of ITS and trnl-F sequences
was first aligned using the algorithm of the program
ClustalX (Thompson et al.. 1994) and then adjusted
manually using the options of the program Se-Al v.
1.0 alpha 1 (Rambaut, 1996). The boundaries of
the ITS region. (ITS1-5.8-ITS2) were determined
according to those established by Hsiao et al.
(1995) for the Pooideae; those of the trnL-F region
(urn intron-trnL 3 exon-trnL-F spacer) were estab-
lished according to the chloroplast map of Oryza
sativa (Hiratsuka et al.. 1989). Gap indels were
coded as binary characters by their presence/ab-
sence (0—1 matrix). Only those gaps that were un-
ambiguous and potentially informative (Torrecilla &
Catalán, 2002) were added to their correspondent
sequence matrix and used for phylogenetic analy-

sis.

134

Annals of the
Missouri Botanical Garden

PHYLOGENETIC
ESTIMATION, AND SEQUENCE

RECONSTRUCTION, RATE
DIVERSITY

Phylogenetic analyses were based on both Par-
simony and Bayesian inference approaches as a
means to compare topologies obtained from cladis-
tic and nucleotide substitution-model-based meth-
ods. The ITS and trnL-F data sets were constructed

and subjected to separate analyses. A first set of

searches was carried out by both excluding and in-
cluding polyploid taxa from the analyses with the
intention of clarifying the placement of the poly-
ploid lineages with respect to their potential an-
cestral diploids by superimposing the polyploids on
the diploid-based trees. A second round of analyses
was conducted excluding gap characters with the
aim of evaluating the phylogenetic signal and influ-
ence that ITS and traL-F indels could have in the
final trees. Finally, a third seach was accomplished
exclusively with the ITS data set excluding the
highly variable sequence of Cutandia maritima
from the analysis (see Results). All the searches
that were conducted exclusively with the diploid
data sets resolved the same topologies as those con-
ducted with the complete data sets (diploids and
polyploids included) for their common taxa (dip-
loid) and showed similar levels of support for their
respective clades; therefore, only trees obtained
from the complete data matrices will be shown
here. ITS trees were the same when gap characters
were either included or excluded from the analyses:
however, an increased lack of resolution was found
for some lineages in the trnL-F parsimony-based
tree when one informative gap indel was removed
from analyses (see Results). Exclusion of Cutandia
maritima. from the ITS data set did not alter the
resulting topologies or their respective levels of
support.

Cladistic analyses were performed with Paup*
ver. 4.0 beta 10 (Swofford, 2002) following the par-
simony criterion. Each data matrix was separately
subjected to two heuristic search strategies aimed
to find putative isles of equally parsimonious trees.
All most parsimonious trees obtained from these
separate searches (search #1: closest, TBR, MUL-
PARS ON; search #2:
10,000 replicates, TBR, MULPARS OFF, saving no
more than 5 trees of score > 10 per replicate) were
used to compute the final strict consensus tree.
Bootstrap support for the best trees found under the
parsimony criterion was estimated through 10,000
1985). The TBR-M (Tree
Bisection Reconstruction swapping, MULPARS
OFF) strategy of DeBry and Olmstead (2000) was

applied for these bootstrap searches in order to get

replicates (Felsenstein,

random-order-entry of

accurate bootstrap values while reducing compu-
tational time.
Bayesian inference search was later performed
for the separate ITS and trnL-F data matrices using
Bayes 3.0 beta 3 (Huelsenbeck € Ronquist,
2002).

substitutions models was previously conducted on

A test of goodness of fit for 56 nucleotide

each individual data set using the likelihood ratio
test statistic included in the program Model Test
ver. 3.06 (Posada & Crandall, 1998) that selects
the best substitution model for the given data. The
estimated optimal substitution model for each sep-
arate data set was then imposed in the subsequent
Bayesian analyses. The General-Time-Reversibility
model with 6 substitution types was the available
option in Mr. Bayes 3.0 for those optimal models
(see Results). Separate searches were conducted for
each independent data matrix under the GTR mod-

(4 gamma rate categories) allowing the program
to estimate the likelihood parameters relative to nu-
cleotide frequencies, nucleotide substitution rates,
and gamma shape (proportion of invariable sites
was set to zero concordantly with the best substi-
tution models selected by ModelTest for each in-
dependent ITS and trnL-F data set).

Bayesian analyses were first. performed through
1.000,000 trees generated by the Markov chain
Monte Carlo (MCMC) sampling trees every 100
generations; phylogenies sampled from their pos-
terior probability distribution were then examined
for stationarity in their likelihood values. Sampled
points from generations that did not reach a stable
equilibrium value (Leaché & Reeder, 2002) were
eliminated using the burn-in option of Mr. Ba
3.0. New Bayesian searches of 1,000,000 MC MC
generations were conducted for each separate data
set; topologies sampled from these new searches
were used to construct the respective 50% Major-
ity-Rule consensus trees where the percentage of
times a clade is recovered is interpreted as an es-
timation of robustness.

The Incongruence Length Difference (ILD) test
of Farris et al. (1994) was calculated to determine
if the two data sets (ITS and trnL-F) differ signifi-
cantly from random partitions of the same size. The
TBR-M approach of DeBry and Olmstead (2000)
was applied to compute the significance values of
the test replicates. Although significance was
achieved from this ILD test (see Results) we decid-
ed to unite the two data matrices onto a combined
one and to conduct further phylogenetic analyses
to explore the resolution obtained from the com-
bined analysis and to evaluate topological incon-
gruences for lineages differently supported in the
and

separate and combined trees. The heuristic

Volume 91, Number 1
2004

=
w
сл

Torrecilla et
Phylogenetic Co ee of Vulpia

bootstrap analyses of the combined data matrix
were performed using the same strategies described
above for the parsimony analysis. Bayesian infer-
ence was also conducted on the combined data set
following the same procedure as for the indepen-
dent data matrices but imposing separate substi-
tution models for each partition in the simultaneous
analysis using the options provided Mr. Bayes

Consensus topologies recovered from the above-
mentioned analyses showed differences in branch
lengths for several lineages (see Results). In order
to investigate the differential rates of evolution that
may have been followed by these lineages, we con-
ducted relative rate tests of nucleotide substitutions
see Results) between different sequences or groups
of sequences using RRTree 1.1 (Robinson et a
1998: Robinson & Huchon, 2000).

constrains the test between lineages or groups ol

m
—

This program

sequences (or between pairs of individual sequenc-
es), which are weighted by a given topology. using
Robinson & Huchon.

—

a close outgroup as reference
2000). Rates of substitutions were compared and
tested between the main lineages or groups of lin-
eages resolved by the Bayesian phylogenetic anal-
yses in the separate ITS and trnL-F trees. The test
was restricted to the ingroup taxa using Festuca
pratensis (Festuca subg. Schedonorus). a member of
the close “broad-leaved” Festuca clade. as out-
eroup. Comparisons were also extended to pairs of
individual sequences within and across lineages
with the aim of analyzing the rates of substitutions
for taxa that
branch lengths with respect to other consectional
or close taxa. The Kimura 2-parameter model was
chosen to estimate the rates of substitution between
the ITS and trnl-F non-coding sequences.

Pairwise comparisons between all sequences de-

showed substantial differences in

tected a few cases. mostly related to the ITS data
set. where individual sequences showed increased
rates of substitutions with respect to other consec-
tional, conspecific, or close lineages (see Results).
In order to evaluate if these lineages evolved more
rapidly than other lineages or could represent po-
tential heterologous samples arbitrarily amplified
from direct PCR reactions we analyzed the % G +
C content of their ITS] regions. which showed to

be the most variable in all the studied taxa. and

estimated the minimum-free energies (MFE) of
folding of their respective RNA transcripts using
the program MFOLD ver. 3.1 (Zuker, 1989; Ma-
thews et al., 1999: Zuker et al., 1999). Folding cal-
culations were set to the default parameters for
RNA sequences (37°С. 5% of thermodynamic op-
timatility) and were made at the M. Zuker web site

(http://ww w.bioinfo.rpi.edu/applications/mfold/old/

rna/form L.cgi).

RESULTS
DNA SEQUENCES
The ITS
from 592 bp (Dactylis glomerata) to 613 bp (Bra-
chypodium distachyon), or 599 bp (Vulpia sicula) to
610 bp (Vulpia fontqueriana, V. membranacea. V.
unilateralis, Psilurus incurvus) within the ingroup
The aligned data matrix consists of 634 po-

sequences of the studied taxa ranged

laxa.
sitions after the introduction of gaps. which ranged
from | bp to 4 bp. Three hundred fifty-two out of
634 nucleotide positions are variable (55% of the
total): of these 147 are located in the ISI region

3%). 38 in the 5.88 gene region (6%). and 167
in the ITS2 region (269€). Of the variable positions
208 are potentially informative (33% of the total)
(94 (15%) in the ITS], 19 (3%) in the 5.85 gene.
95 (15%) in the ITS2).

The Vl data matrix ranged from 779 (Puc-
cinellia distans) to 908 (Secale cereale) or 819 bp
(Festuca rothmaleri) to 848 bp (Psilurus incurvus.
Micropyrum tenellum) within the ingroup taxa. The
aligned data matrix is made of 1022 positions after
the introduction of gaps that varied from 1 bp to
32 bp (a 64 bp deletion in Puccinellia distans). The
rate of variability and potential phylogenetic infor-
mativeness of the chloroplast trnL-F region is lower
than that of the nuclear ITS region for a similar set
of taxa. In the trnL-F region 323 out of 1022 po-
sitions are variable (32% of the total), and of these
164 (10%) are located in the tral intron, 11 (1%)
are located in the tral 3“ exon. and 148 (15%) in
the trnL-F spacer. Of 323 total variable sites, 131
are potentially informative (12.5% of the total) (76
(7.3%) in the trnL-F intron, 2 (0.2%) in the iral
3’exon, and 53 (5%) in the trnL-F spacer).

PHYLOGENETIC ANALYSIS

The ITS Data Set
The first heuristic search found one island
213.592 equally parsimonious trees that were 950
steps long. CI = 0.409 excluding uninformative
characters, RI = 0.010.
dered 6631 equally parsimonious trees of the same

The second strategy ren-

length and statistics as the previous ones. The strict
consensus tree of all these most parsimonious trees
is shown in Figure 1.

A monophyletic FEstuca sensu stricto + Vulpia
+ Related Ephemerals (FEVRE) group that encom-
passes Festuca sects. Eskia, Festuca, Aulaxyper and

subsection Exaratae; Vulpia sects. Vulpia. Monach-

136

Annals of the

Missouri Botanical Garden

95

100

50

pescao
л
N

Eyad | 2 . eite brad
100

56
83

=

Figure 1. ITS

uninformative characters,

RI =

corresponds to a highly variable sequence of (

Results and Discussion).

Festuca rothmaleri

Festuca rubra (2)
Festuca rubra (1)
Festuca juncifolia
Festuca rivularis

Vulpia fasciculata (1)
le ا‎ (2)

Cutandia maritima (*)
Vulpia AS
Vulpia membran
Festuca ongiauriculata
Festuca ov

Festuca ри ИЗ

Vulpia ciliata (2)
Psilurus incurvus
Vulpia unilateralis (1)
Vulpia unilateralis (2)

Festuca capillifolia
Festuca clementei
Ctenopsis уп tula
Narduroides salzmannii
Festuca e
Festuca gautieri
Festuca eskia

Festuca quadriflora

lium perenn
pate. 1
Festuca altissima
Dactylis glomerata
Puccinellia distans
Poa infirm
Se а еа
Secale

L FL I Ll

Br 5 distachyon

0.610). Bootstrap percen

tage is indice

Schedonorus + Lolium

меа c
4 maritima that was both included and е
Species numbers correspond to different accessions of the same taxon (see Table 2

—

FEVRE

Aulaxyper
(red fescues)

Micropyrum

Vulpia p. p.
(diploid)

Spirachne
Monachne
Loretia

Cutandia

Festuca plicata

estuca
(F. ovina fescues)

Psilurus
Vulpia p. p.
(polyploid)

Apalochloa

Exaratae

Eskia

„„ „„ „„ „„ „„ „„ mmm mmm mm mm mm mm mm mm e e e mm mm mm mm

Drymanthele

tree: strict consensus tree of 213,592 equally parsimonious trees (L = 950, CI = 0.469 exc luding
isk

m the Pep чи branches. Aster

xcluded from analyses ae
2).

Volume 91, Number 1
2004

Torrecilla et al. 137

Phylogenetic Relationships of Vulpia

ne, Spirachne, Loretia, and Apalochloa; and Psilu-
rus, Ctenopsis, Wangenheimia, Cutandia, Micropy-
rum, and Narduroides is obtained when
Brachypodium distachyon is used to root the trees.
The first diverging lineages of the FEVRE group
are those corresponding to Festuca sect. Eskia. This
taxon forms a non-resolved basal assemblage of five
species (see Fig. 1). The core of the FEVRE taxa
is also unresolved at the base: five clades collapse
with seven single taxa in a polytomy. These termi-
nal taxa are those belonging to Festuca subsect.
Ё. xaratae (Е borderet,

Narduroides,

F. clementer,

F. capillifolia).
pyrenaica, Wangenheimia, and
Ctenopsis. Of the five resolved clades one repre-
sents the Aulaxyper + Micropyrum + diploid Vul-
pia (diploid Vulpia sect. Vulpia) lineage. Micropy-
rum is resolved as sister of Festuca sect. Aulaxyper.
though this relationship is poorly supported: this
group is respectively sister to the diploid Vulpia
sect. Vulpia clade. High bootstrap support is shown
for the separate lineages diploid Vulpia (bs 100),
Micropyrum (bs 99), and the sister taxa Festuca
+ Ё

clade is resolved into two diverging lineages of in-

nevadensis rothmalerí (bs 95). The second
termixed representatives of Vulpia sects. Spirachne.
and Loretia plus Cutandia and Festuca
(Vul-
pia membranacea + V. fontqueriana)) subclade is
well supported, whereas the ((Vulpia brevis + V.
sicula). V. geniculata) subclade is
mostly robust throughout.
the Festuca taxa with relatively high bootstrap sup-
port A fourth

Psilurus + polyploid Vulpia (polyploid Vulpia sect.

Monachne.
plicata. The ((Vulpia alopecuros Cutandia).

fasciculata), V.
A third clade is that of
(bs 84) but little internal resolution.

Vulpia) clade is also highly supported (bs 99); Psi-
lurus is resolved as the closest relative of a clade

of Vupia representatives where two sister accessions
of V. myuros (bs 83) collapse in a polytomy with
two representatives of V. ciliata (bs 81). The fifth
clade is that of two representatives of Vulpia uni-
lateralis (bs 87) (Vulpia sect. Apalochloa).

Model Test found TrN + G to be the best substi-
tution model for the ITS data matrix. The Bayesian
analysis conducted under the GTR model (nst = 6.
ріпу = 0) sampled 8927 trees that reached a stable
likelihood value after the burn-in of 1074 trees; the
50% majority rule consensus tree of. all sampled
trees is shown in Figure 2. The phylogenetic rela-
tionships recovered in this tree are similar to those
shown in the parsimony-based tree for the best sup-
ported groups (Fig. 1). notably those corresponding
to the basal Eskia group, and to the internal clades
Aulaxyper + Micropyrum diploid Vulpia, Spi-
rachne + Monachne + Loretia + Cutandia + F.
plicata, Festuca, and Psilurus + polyploid Vulpia.

The Apalochloa clade is nested within a elade of
ephemeral taxa (including Wangenheimia, Narduro-

ides, and Ctenopsis) in this Bayesian tree.

The trnl-F Data Set

The first heuristic strategy found one island of
1.094.005 equally parsimonious trees that were
533 steps long, CI = 0.610 excluding uninforma-
tive characters, RI = 0.778.
rendered 3838 equally parsimonious trees of the

The second search

same length and statisties as previously. The strict
consensus tree of all these most parsimonious trees
is shown in Figure 3. The trnL-F strict consensus
topology shows a slightly higher resolution for the
deep internal branches of the core taxa than that
of the ITS strict consensus topology (Fig. 1) though
they remain poorly supported. The consensus to-
pology was less resolved for representatives of Vul-
pia sects. Spirachne, Monachne, and Loretia and
related ephemerals and for those of Festuca sub-
sect. Exaratae and allies when gap characters were
excluded from analysis (results not shown). Four of
the five gap characters constitute additional mark-
ers for clades already supported by substitution

changes: however, a fifth gap shared by represen-

atives of Vulpia sects. Spirachne, Monachne. Lor-
etia, and Apalochloa plus Cutandia, Festuca pli-
cata, Festuca subsect. Exaratae, E pyrenaica and
F. clementei is the only character that supports the
monophyly of this group in the parsimony-based
tree (Fig. 3). Nonetheless. the Bayesian inference.
which is solely based on nucleotide sequences (Fig.
4). recovers a similar topology to the parsimony
based one.

The trnL-F data set also confirms the monophyly
of the FEVRE group, which is supported by a high
bootstrap value (bs 94) (Fig. 3). Within this clade
representatives of Festuca sect. Eskia are paraphy-
letic and basal to a core of fine-leaved fescues, Vul-
pia, and related annual genera (Fig. 3). In this tral -
Е topology, Festuca burnatii and F quadriflora
separate earlier from the common ancestor but are
unresolved, being followed by the divergence of the
remaining Eskia taxa (А eskia, E gautieri, Е ele-
gans) that collapse in a polytomy and are sister to
the rest. The core of the FEVRE taxa is formed by
three lineages that collapse in a further polytomy.
The best resolved lineage is the one that encom-
passes the "rubra and ovina” fescues and their al-
lies (bs 92). Within this group the Aulaxyper
diploid Vulpia clade is well supported (bs 97). The
clade is sister to the Festuca + Wangenheimia one
(bs 92) where the Festuca subclade shows a high
bootstrap value (bs 99). Narduroides is resolved as

138

Annals of the
Missouri Botanical Garden

FEVRE

Festuca rothmaleri
ensis

Mic P tenellum
Micropyrum patens

Vulpia muralis (1)
Vulpia muralis (2)

Vulpia bromoides

Vulpia fasciculata (1
ulpia fasciculata (2)
ulpia brevis

«€

Vulpia sicula
Vulpia geniculata
Vulpia alopecuros

Vulpia fontqueriana
Me ds membranacea

Festuca plic
Vulpia unilateralis
Vu

— Festuca bor

— Festuca Dna

— Festuca clementei
Festuca longiauriculata

Cutandia maritima (*)

antral mol Apalochloa

Festuca
(F. ovina fescues)

Aulaxyper
(red fescues)

Micropyrum

Vulpia p. p.
(diploid)

ш $рїгасһпе
Мопасһпе
Loretia
Cutandia

Festuca
plicata

99 Festuca hystrix
Festuca frigida
Festuca alpina —
- Festus capillifolia
73 Vulpia myuros (1)
99 I Vulpia myuros (2) Psilurus
100 Vulpia ciliata (1) Vulpia p. p.
90 Vulpia ciliata (2) bloi
Psilurus incurvus (polyploid)
Festuca elegans
— Festuca burnatii
Festuca eskia Eskia
Festuca gautieri
SEB BB Bae EEE ERER ow a ann SEB BBB SBSBRB SSBB RBRBRB BBB eeee

""""mmuamu
00

olium perenne
Festuca pratensis
Festuca altissima
Dactylis glomerata
Puccinellia distans

oa infirma

Schedonorus + Lolium
Drymanthele

Sesleria argentea
Secale cereale
Brachypodium distachyon

0.1

Figure 2.

is indicated on the corresponding branche

Ast

ITS tree: Bayesian 50% e Rule (MR) consensus tree of 8927 trees. Posterior probability percentage

erisk corresponds

to a highly variable sequence

e of C.

maritima that

was both included and excluded from a "s (see Results and Discussion). Species numbers correspond to different

as?

Table 2).

accessions of the same taxon (see

Volume 91, Number 1
2004

Torrecilla et al.
Phylogenetic Relationships of Vulpia

Un
—

—
= un

r2
—

Vulpia unilateralis (1)
Vulpia unilateralis (2)
Vulpia sicula
Vulpia alopecuros
Cutandia maritima
iie borderei
a pyrenaica
Festuca capillifolia
estuca clementei
2 m
Vulpia brevis
Vulpia fasciculata (1)
Vulpia fontquerana
bob a membranacea
Vulpia geniculata
Ctenopsis delicatulá

67

Vulpia bromoides

:

Festuca rothmaleri
Festuca juncifolia
Festuca nevadensis

Wangenheimia lima
Narduroides salzmannii

Psilurus incurvus
Vulpia ciliata (1)
Vulpia ciliata (2)

I
ا‎ e SEN

um perenn
Festuca pratensis
Festuca altissima

actylis glomerata
Puccinellia distans

Poa infirma

Sesleria argent
Brachypodium айне оп

Secale cereale

Figure 3.

rs,

RI

= (0.778). Bootstrap percentage is

numbers correspond to different accessions of the same taxon (see

indic

ö NVI E еее...

trn L-F tree: strict consensus tree of 1,694,605 equally parsimonious trees (L

uninformative characte ated

Table 2)

.20£. .0.0000000xX0xX 000 0£. LC CTA

FEVRE

Aulaxyper
(red fescues)

Vulpia p. p.
(diploid)

Festuca
(F. ovina fescues)

Wangenheimia

Spirachne
Monachne
Loretia
Cutandia
Festuca plicata
Apalochloa
Ctenopsis

Exaratae

Psilurus
Vulpia p. p.
(polyploid)

Micropyrum

Eskia

Schedonorus + Lolium
Drymanthele

on the corresponding branches, Spee

= 533, Cl = 0.610 exc luding

140 Annals of the
Missouri Botanical Garden

Leere bci SCR.
a 9 Festuca rothmaleri | в
= FEVRE Festuca juncifolia
в Festuca nevadensis Aulaxyper a
: Festuca rivularis (red fescues) s
1 ulpia bromoides a
в Vulpia muralis (1)
: ا‎ non ie ulpia p. p.
и а
= жеди Hae
в
: estuca айша ^
aragonensis Festuca
Festuca hystrix (F. ovina
Festuca indigesta fescues)
stuca frigida ч
Festuca glacialis Wangenheimia
; Wangenheimia lima
: 80 Narduroides salzmannii
. Psilurus incurvus А :
: Vulpia ciliata (1) PUE
к Vulpia ciliata (2) Vulpia p. p. ]
" Vulpia ciliata (3) (polyploid) :
: Vulpia myuros (1) :
. cropyrum tenellum Micropyrum
: Micropyrum patens 2
= 100 Vulpia alopecuros Apalochloa
= 55 fb cu Cut ч aridus |
= 60 Vulpia bre Spirachne
a Vulpia иин (1) Мопасһпе
= 1 Vulpia unilateralis (2) |
м Vulpia sicula Loretia а
100 r '
a 89 Vulpia fontquerana |Cutandia *
: b. Vulpia membranacea WE-
- ا‎ ы fasciculata (1) Ctenopsis
Vulpia geniculata Festuca
Ctenopsis delicatula Е plicata
Festuca plicata
Festuca clementei
Festuca border
Festuca pyren Exaratae
pyrenaica в
Festuca capillifolia :
Festuca gautieri a
: Festuca eskia И
- Festuca elegans Eskia -
s Festuca burnatii e
А =... Festuca MALA a a « IA A AI
100 Loliu

m perenne
Festuca pratensis Schedonorus + Lolium

Festuca altissima Drymanthele

Dactylis glomerata

Sesleria argentea

Puccinellia distans

a infirma

Brachypodium distachyon

1

Figure 4. trnL-F tree: Bayesian 50% MR consensus tree of 9890 trees. Posterior probability percentage is indicated
on the corresponding brane hes Species numbers correspond to different accessions of the same taxon (see Table 2).

Volume 91, Number 1
2004

Torrecilla et al. 141

Phylogenetic Relationships of Vulpia

the sister taxon of the former groups but this rela-
tionship shows low bootstrap support (bs 56) (Fig.
3). A second lineage of Psilurus + polyploid Vulpia
shows relatively high support (bs 85): Vulpia myu-

ros is resolved as sister to an unresolved clade of

Psilurus and Vulpia ciliata representatives with low
bootstrap support (bs 67). A highly robust Micro-
pyrum clade includes the sister taxa M. tenellum
and M. patens. This clade is resolved as sister to
the Psilurus + polyploid Vulpia lineage though this
relationship lacks bootstrap support. The third lin-
eage includes representatives of Vulpia sects. Spi-
rachne. Monachne, Loretia, and Apalochloa. Cutan-
dia, Ctenopsis, Festuca plicata. and Festuca sect.
F. cle-

This group is poorly re-

Exaratae (F. borderei, F. capillifolia) plus
тете and H. pyrenaica.
solved and not strongly supported except for the
relationships of the sister taxa Vulpia alopecuros +
Cutandia maritima (bs 79). Vulpia unilateralis (Vul-
pia sect. Apalochloa) is resolved here as sister to
Vulpia sicula though their relationship is not sup-
ported (Fig. 3).

The goodness of fit test of ModelTest indicated
K8luf + G as the best substitution model for the
trnL-F The

ducted under the GTR model (nst = 6. рту = 0)

data matrix. Bayesian analysis con-

sampled 9890 trees that reached a stable likelihood
value after the burn-in of 111 trees: the 50% ma-

M?

jority-rule consensus tree of all sampled. trees i
shown in Figure 4. The phylogenetic relationships
recovered by this analysis are congruent with those
based in the parsimony approach, as manifested in
the two topologies depicted in Figures 3 and 4. All
eroups except the unresolved Festuca sect. Exara-
tae taxa plus E clementei and К pyrenaica show
congruence in both parsimony and Bayesian trees.

The Combined ITSArnL-F Data Set

Parsimony strict Consensus topologies and
Bayesian 50% majority-rule consensus trees ob-
tained from the two separate data sets. ITS and
trnL-F.. were coincident for several groups. espe-
cially for the best supported lineages Aulaxyper +
diploid Vulpia. Festuca. Psilurus + polyploid Vul-
pia. and Spirachne + Monachne + Loretia + Cu-
tandia + F. plicata and for the basal position of
1—1).

that both the nuclear and the chloroplast genomes

section Eskia (Figs. These results indicate
recover a similar phylogenetic signal for most of the
studied taxa. Incongruences between the ITS and
trnL-F trees refer to the distinct placement of Vul-
pia sect. Apalochloa, as well as Wangenheimia, Mi-
cropyrum, and Narduroides.

To clarify the evolutionary relationships of those

eroups and to improve the resolution of the final
tree we decided to unite both data matrices into a
combined one and conduct further simultaneous
phylogenetic analysis on the enlarged data set. A
combined ITS/trnL-F
samples that were sequenced for the two molecules:
the ILD test of Farris et al. (1994) carried out on
this ITS/trnL-F data matrix indicates that the two
data sets are significantly different from two random

їл

data matrix was made of 5:

partitions of the same size as the original data ma-
trices (1000 replicates; Р = 0.001).
about the validity that heterogeneity detected. by

Arguments

the test between sequence data matrices may have
in terms of their combinability have been various
(Davis et al., 1998; Johnson & Soltis. 1998: Yoder
et al., 2001: Barker & Lutzoni, 2002). Davis et al.
(1998). Yoder et al. (2001). and Barker and Lutzoni
(2002) considered the ILD test an inappropriate
method to test for the combination of data partitions
for simultaneous analyses: the latter authors further
demonstrated the poor predicting value shown by
the ILD test for data set combinability intended to
increase phylogenetic accuracy even at critical val-
ues as low as P = 0.001

The first heuristic search found one island of 577

equally parsimonious trees that were 1488 steps

long. CI = 0.503 excluding uninformative charac-
ters. RI = 0.644. The second strategy rendered 686

equally parsimonious trees of the same length and
statistics that enlarged the spectrum of equally par-
simonious trees. The strict consensus tree of all
these most parsimonious trees is shown in Figure 5.

The strict consensus [TS/trnL-F tree depicted in
Figure 5 is resolved for the main FEVRE groups:
this FEVRE clade shows strong bootstrap support
(bs 100) and

divergence of the basal section Eskia taxa (Fig. 5)

resolution is obtained here for the

and for the branching of some internal core FEV RE
lineages. The two representatives of Vulpia unila-
teralis join in a well supported monospecific Apal-
ochloa clade (bs 99) that is resolved as sister to
Ctenopsis and then to the Spirachne + Monachne
+ Loretia + Cutandia + F. plicata clade though
The Mi-

cropyrum taxa also join in a congeneric clade that

none of these relationships is supported.

shows strong bootstrap support (bs 100). The com-
bined ITS/trnL-F tree shows only a partial resolu-
tion for the relationships between the core FEVRE
groups. The best resolved lineage is that of the Au-
laxyper + diploid Vulpia and the Festuca + Wan-
genheimia groups, which link together in a clade
that is sister to Narduroides; however. these rela-
tionships lack bootstrap support. Internal resolution
is absent for the remaining lineages. except for a

clade that shows a paraphyletic basal divergence of

142

Annals of the

Missouri Botanical Garden

12 7 772 22 — —— 2 2 K 2 „ „„ „„ „„ „„ „% „„ % nnn MMB By,
a B
z Festuca rothmaleri (8x) — FEVRE :
1 Festuca nevadensis (10x) м
: Festuca juncifolia (8x) Aul в
: Festuca rubra (2) (6x) ee "
. Festuca rubra (1) (6x) (red fescues) s
: Festuca iberica (6x) :
: Festuca rivularis (2x) Vulpia p. p. Р
a Vulpia muralis (1) (2x) (diploid) .
: Vulpia muralis (2) (2x) :
. Vulpia bromoides (2x) "x a
: Festuca hy (2x) e =
: Festuca longiauriculata (2x) estuca :
в Festuca aragonensis (4x) ; a
. т ER тга (2х) (Е. ovina fescues) .
" Festuca alpina (2x) Wanvenheimi a
в Ll genheimia в
. 76 Festuca glacialis (2x) .
: Festuca frigida (2x) :
. Wangenheimia lima 2x) — в
: Narduroides salzmannii (2x) :
x Vulpia alopecuros (2x) — =
s Cutandia maritima (2x) Apalochloa a
я Vulpia fontqueriana (2x) Spirachne :
= Vulpia membran (2x) :
Ы Vul vis (2x) Monachne в
9 Vulpia fasciculata (1) 4x) ; в
: Vulpi la Go l Loretia “
ы Vulpia geniculata (2x Cutandia :
в Festuca plicata 2x) .
в Vulpia unilateralis (1) (2х) Ctenopsis a
: Vulpia unilateralis (2) — (2x) | :
a Ctenopsis delicatula (2x) — Festuca plicata .
м Festuca borderei (2x) = ч
в Festuca pyrenaica 4x =
А Festuca capillifolia a І Exaratae :
= Festuca clementei (2x) — :
a Vulpia myuros (1) (6x) — Psilurus =
в Vulpia ciliata (1) (43) Vulpia p. p. в
E Vulpia ciliata (2) (4x) me .
е Psilurus incurvus (4x) — fporplaun :
ы Micropyrum tenellum (2х) : :
н Місгоругит patens (2х) — Micropyrum н
= Festuca elegans 2x) z
: Festuca burnatii (2x) =
. Festuca gautieri cR Eskia s
: Festuca eskia е
2 Sea BEeBBBB BSB Peace Яра ог паш (x) "uuu EIE и пашшшшшшшшпшппшпшпшшпвшпшыш Es
90 со, Schedonorus + Lolium
52 Festuca altissima — Drymanthele
100 Dactylis glomerata
Sesleria argente
Puccinellia distans
Poa infirm
Secale cereale
E Brachypodium distachyon
Figure 5. Combined ITS/trnL-F: strict consensus tree of 686 equally parsimonious trees (L = 1488, CI = 0.503

excluding uninformative characters, RI =
Species number

).644). Bootstrap percentage is indica

tree; black bars correspond to polyploid lineages

ted on the corre аралаш branches.

's correspond to different accessions of the same taxon (see Table = Ploidy levels are mapped into the

Volume 91, Number 1
2004

Torrecilla et al. 143

Phylogenetic Relationships of Vulpia

the Festuca subsect. Exaratae taxa plus E pyren-
aica and E clementei from the topology for the core
group of Vulpia taxa and their allies (Fig. 5).

The Bayesian simultaneous analysis conducted
under the GTR model (nst = 6, pinv = 0) sampled
9643 trees that reached a stable likelihood value
after the burn-in of 358 trees; the 50% majority
rule consensus tree of all sampled trees is shown
in Figure 6. Relationships recovered by this anal-
ysis are mostly congruent with those based in the
parsimony approach: however, a polytomic assem-
blage of Festuca subsect. Exaratae taxa plus Е pyr-
enaica and E clementei taxa are resolved here as
the the FEVRE

whereas the Psilurus + polyploid Vulpia clade and

basal lineages of core group.
the Micropyrum clade collapse in a polytomy with
the “Festuca rubra and ovina” group plus allies.
Rates of Substitutions and Sequence Diversity
between FEVRE Lineages

Values and levels of significance of the relative-
rate tests calculated between the main FEVRE lin-
enges for the separate ITS and trnL-F sequences
are shown in Table 3. Rates of substitutions vary
the ITS

reflecting the less constrained nature of the

тоге for sequences than for the trnL-F
ones,
ribosomal nuclear region compared to the con-
served one of the chloroplast genome. Overall. pe-
rennial lineages show significant lower rates of sub-
stitution than the annual ones for both ITS and
irnL-F sequences; however, most of these low rates
are contributed to by representatives of the Eskia
group. which show significant differences to almost
all other FEVRE lineages for both genomic regions.
When the Eskia taxa are removed from the test. the
core FEVRE perennial lineages evolve, in general
terms, at a slower pace than the core FEVRE an-
nual ones but the differences are not significant.
Pairwise comparisons between individual sequenc-
es show Festuca elegans to be the fastest evolving
lineage within the otherwise slow evolving assem-
blage of Eskia taxa (results not shown).

The core FEVRE perennial groups. also. show
marked differences in their respective substitution
rates; the Exaratae group evolves slower, followed
by the intermediate rate of the Festuca lineage and
the more rapidly evolving rates of the Aulaxyper
lineage (Table 3). Significant differences in substi-
tution rates between the Exaratae group and the
ITS and the ul se-
quences though they are restricted only to the ITS

annuals occur for both the

set in several Festuca to ephemeral-groups com-

^

parisons. The Aulaxyper lineage shows higher sub-
stitution rates than those of the other perennial

firma, 50.5%).

groups and evolves only slightly slower than most
of the annual lineages except for the Loretia assem-
blage ITS sequences. This group evolves faster but
not significantly more so than the red fescues if
Cutandia maritima is excluded from the analysis
(Table 3) (see Discussion). Pairwise comparisons
between individual sequences found F rothmalert
to be a fast-evolving lineage within the Aulaxyper
group with rates significantly higher than those of
other consectional taxa like E juncifolia and F ri-
vularis in both ITS and trnL-F sequences. Similarly.
F. frigida also shows significant higher substitution
rates than those of the remaining cosectional Fes-
tuca taxa for the ITS sequences and than those of
F. alpina and E. clementel for the trnL-F sequences
(results not shown).

Within the group of FEVRE annuals the Loretta
assemblage and Ctenopsis delicatula are the most
rapidly evolving lineages with respect to the chlo-
roplast V sequences, being significantly faster
than the Apalochloa, Micropyrum, and Wangenhet-
mia lineages and than the Apalochloa, Micropyrum,
and Psilurus + polyploid Vulpia groups respectively
(Table
cantly faster than the diploid Vulpia and the Nar-

The Loretia group also evolves signifi-
duroides lineages for the ITS sequences if Cutandia
maritima is included in the group but shows no sig-
nificant differences to those lineages if this taxon is
(Table 3) (see Dis-

cussion). Analvsis of pairwise comparisons between

excluded. from the calculations

individual ITS sequences pointed to Cutandia mar-
imd as the fastest-evolving taxon of the FEVRE

clade for this genomic region: differences lo rates

shown by other taxa were significant in all cases
except for the Festuca rothmalert, Vulpia fontqueri-

ana, and И membranacea ones (results not shown).

The % G + C content and the free energy «
folding of the ITS] region showed some differences
among the studied taxa. The average percentage of
guanine and cytosine residues was 00.5% for the
ingroup taxa; however, slightly lower values were
observed for the annual taxa (from 50.8% in Vulpia
membranacea to 58.7% in V. alopecuros) than in the
perennial ones (from 60.4% in Festuca rivularis to
Cutandia maritima
(54%),

this percentage is similar to that of other

D
de

n V. quadriflora).

—

showed the lowest content of G + C though
variable
ingroup and outgroup annual species (1.e.. Poa in-
The variable perennial taxon Fes-
tuca rothmaleri had a percentage of 59%, close to
the perennial outgroups F pratensis and Lolium
perenne (58%). Average Minimum Free Energy
(МЕЕ) of folding of the ISI RNA transcripts was
—87.60 kcal/mol (sd = + 6.96 keal/mol) for the

ingroup taxa. Folding energies also showed slight

144 Annals of the
Missouri Botanical Garden

AAA „„ „ „ „ „ AAA AAA DBS 8 и

FEVRE 51 Fes 0 um
{ Ашахурег
(гед fescues)

Vulpia р. р.
(diploid)

Festuca
(F. ovina
fescues)

Wangenheimia

Psilurus
Vulpia p. p.
(polyploid)

ulp
Psilurus incurvus

TL Micropyrum tenellum
Micropyrum patens ] Micropyrum
00 —

Vulpia alopecuros

utandia maritima
Vulpia fontqueriana Spirachne
Vulpia membranacea

Apalochloa

Vulpia brevis Monachne
Vulpia deii (1) Loretia

Vulpia |

Vulpia MEN Cutandia

tuca plicata Ctenopsis
Festuca
Ctenopsis delicatula SJ plicata
— Festuca borderei
— Festuca pyrenaica
96 — Festuca capillifolia

Exaratae

[- Festuca gautieri

гү eskia Eskia
a burnatii

MT 2Q0¿»n£0.%.0X000.L..LAÚLRwf E .s0 0000205000005»

б у idi Schedonorus + Lolium

aaa altissima Drymanthele

actylis glomerata

Sesleria argentea
Puccinellia distans
Poa infirma

Secale cereale
1 distachyon

0.1

Figur Combined ITS/trnL-F: Bayesian 50% MR consensus tree of 9643 trees. Posterior probability 5
is nic М 100 on the corresponding branches. Species numbers correspond to different accessions of the same taxon (se

Table

145
Phylogenetic Relationships of Мира

Torrecilla et al.

Volume 91, Number 1

2004

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Annals of the

146

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Volume 91, Number 1
200

Torrecilla et al. 147
Phylogenetic Relationships of Vulpia

Continued.

Ra

Table

Jil
sd-dK

sd-dk

Group 2

Group |

0.03 1688*

0.006411
0.005912

0.006618
0.007721

0.0002
0.00212

773

0.013

0.431212
0.854749
0.60759

0.01 1353

0.008936

0.001

Psilurus + Vulpia (polyploid)

Ctenopsis

Ipalochloa

Ctenopsis

0.009983**
0.238803
0.057241

0.012093

0.00021
0.01298

Ctenopsis

0.009095
—0.011935

)

<

”

Varduroide:

ad

5

0.41871

0.01 1648

0.009419

Wangenheimia

Ctenopsis

0.01 8459*

— 0.004990

0.006659 0.000159:

—0.025183

7 annuals

"fine-leaved

‘fine-leaved”

perennials

VRE

8.45 + 00**
1.1 4E +00%*

0.209934

0.002816
0.002995
0.002113

í

0.01108

0.001 502**

0.000200

0.00

0.019636
0.031168

0.0092

Eskia
Eskia

l perennials

4

FE

?

0.0132 1%
0.00233]!

1.38E —03**

5981
0.005389

72

0.0850

9

4

Core FEVRE annuals

Core FEVRE

perennials

—

differences between annual and perennial taxa
though the spanning ranges overlapped across sev-
eral taxa. The perennial lineages had general
from — 100.20
kcal/mol in Festuca quadriflora to = 78.00 kcal/mol

=

more stable predicted. structures

in F. rubra) than the annual ones (from —98.10
keal/mol

mol in Micropyrum patens). Cutandia maritima re-

in Wangenheimia lima to — 19.00 kcal/

flected the poorest folding dynamic (= 70.50 kcal/
mol) of all analvzed taxa though Festuca frigida and
other outgroup taxa also showed high МЕЕ values
(E frigida = —71.60 kcal/mol. Dactylis геа
= — 72.00 kcal/mol, Poa infirma = 3.4 keal/

mol).

DISCUSSION

CIRCUMSCRIPTION OF FEVRE. POLYPHYLY OF VULPIA
AND PARAPHYLY OF THE FINE-LEAVED FESTUCA

One of the main conclusions of this study is the
confirmation that FEVRE is a complex group that
includes not only all lineages of Vulpia and the four
of fine-leaved Festuca, as considered herein, but
also the annual genera Psilurus, Wangenheimia.
Ctenopsis. Micropyrum, Narduroides, and Cutandia.
This group is monophyletic and well supported and
clearly differentiated from the “broad-leaved” Fes-
tuca and from other sampled Poeae that have been
used here as outgroups (Figs. 5 and 6).

It is also relevant to have demonstrated that the
genus Vulpia, as presently constituted, is a poly-
phyletic assemblage of at least four distinct line-
ages. Conversely to what has been found for Lol-
ium

a monophyletic group of taxa likely derived

from a Festuca pratensis ancestor (Charmet et al..
97; Gaut et al.. 2000:

2002)—the Vulpia taxa do not share a common an-

Torrecilla & Catalán.

cestry but have had independent origins within the
fine-leaved fescues.

ithin Festuca, the paraphyly of the different
fine-leaved lineages has been shown. most inter-
estingly in respect to the separate placement of the
subsection Exaratae taxa versus sections Festuca
and Aulaxyper taxa. The two groups include species
with both intravaginal and extravaginal (or mixed)
innovation shoots although they fall in different
clades of the tree.

THE BASAL SECTIONS ESKIA AND PSEUDATROPIS

Section Eskia is shown to be paraphyletic, the
representatives constituting the earliest-diverging
lineages of the FEVRE clade. This basal position
of the group is concordant with the extremely low
substitution rates accounted for by its members.

148

Annals of the
Missouri Botanical Garden

Festuca elegans, classified in the monotypic section
Pseudatropis by Krivotulenko (1960), is shown to
je the closest relative of the core FEVRE taxa
(Figs. 5 and 6), a result that is also correlated with
the higher substitution rates accumulated by this
species in its ITS genome. All the five taxa are
mostly endemic diploids of the western Mediterra-
nean area. They have been classified in Festuca
sect. Eskia Willk. p.p. (= sect. Variae ser. Intra-
vaginales Hack.) because they share several ple-
siomorphic traits, such as pubescent ovary apices,
broad scarious margins of glumes and lemma, and
a caryopsis free from the palea.

The consecutive divergence of a resolved lineage
of three species (Festuca quadriflora (F. gautieri
F. eskia)) followed by that of F burnatii in the par-
simony-based tree (Fig. 5) is partially contradicted
in the consensus Bayesian tree where А quadriflora
and F burnatii are resolved as the succesive oldest
lineages of this group (Fig. 6), though none of these
relationships is strongly supported. Both F quad-
riflora and F. gautieri hybridize spontaneously with
F. eskia, which indicates a close genetic relation-
ship among them. Conversely, F burnatii, an iso-
lated endemic from northern Spain that differs mor-
phologically from the other taxa, does not intercross
with any other sympatric member of the Eskia
group. Festuca elegans shares with the above taxa
the overall morphological attributes, being a rela-
tively tall fescue with thin scabrous leaves. Krivo-
tulenko (1960) classified F elegans in its own sec-
tion Pseudatropis based on its glabrous ovary apex,
orbicular to ovate hilum, and elliptic lemma; how-
ever, Torrecilla et al. (2003), in their recent mor-
phological survey of Festuca sect. Eskia and related
allies, demonstrated that the characters used by
Krivotulenko were not stable across the geograph-
ical range of the species, rejecting the separate sec-
tional treatment proposed by this author. The trnL-

data set indicates a close relationship of E
elegans with Е gautieri and F. eskia (Figs. :
4), whereas the ITS data set supports the closeness
of this taxon to the core group of FEVRE (Figs. 1
and 2). The combined ITS and trnL-F analysis pro-

3 and

vides the same sister relationship for F elegans and
the FEVRE core taxa with moderate bootstrap sup-
port. A larger taxon sampling of representatives of
Festuca sect. Eskia and other close groups will be
necessary in order to resolve the phylogeny of the
basal lineages of the FEVRE clade.
VULPIA SECT. VULPIA Р.Р. (DIPLOIDS) AND FESTUCA
SECT. AULAXYPER

One of the best resolved lineages of the tree is
that of Aulaxyper + diploid Vulpia (Figs. 5 and 6),

a clade that shows high bootstrap and posterior per-
centage support for most of its branches. Although
the sampling of representatives of Festuca sect. Au-
laxyper only covers a small percentage of the spe-
cies attributed to this group (Ainscough et al.,
1986) it includes the type species and some of the
typical members of the F rubra complex. The prox-
imity of diploid Vulpia sect. Vulpia taxa (V. muralis,
V. bromoides) to Festuca sect. Aulaxyper is strongly
supported in the trnL-F based topology (Figs. 3 and
4) and less supported in the ITS based one (Figs.
l and 2). The combined ITS and trnL-F data matrix
recovers the same sister relationships as the sepa-
rate data sets and reinforces the robustness of this
clade. Phylogenetic analyses conducted exclusively
with the diploid data sets recovered the same evo-
lutionary links for F rivularis, one of the few dip-
loid representatives of the Aulaxyper group, and the
two diploid Vulpia taxa studied in this survey (V.
bromoides, V. muralis) (results not shown). This Vul-
pia annual lineage could have derived from Aulax-
yper perennial ancestors from which it likely in-
herited its chloroplast genome. The substitution
rates shown by the two groups were similar for both
the ITS and the trnL-F regions, the Aulaxyper as-
semblage being the most rapidly evolving lineage
of all perennial FEVRE groups. The close phylo-
genetic relationships found between representatives
of the red fescues and of diploid representatives of
Vulpia (Figs. 3—6) are partially in
agreement with their assumed genetic relatedness

Vulpia sect.

corroborated by intergeneric spontaneous hybrids
(Ainscough et al., 1986) but strongly contrast with
all current classifications of Vulpia sect. Vulpia
(Cotton & Stace, 1977; Stace, 1981), especially for
the separate evolutionary placements of the respec-
tive diploid and polyploid lineages.

Within Aulaxyper an evolutionary trend from low
2x to 6x—8x—-10x)

and from slender to more robust plants could be

to high ploidy level taxa (2n =

suggested along the clades of the group when the
polyploid species are superimposed on the diploid
tree (Figs. 5 and 6). Festuca rivularis (diploid), a
plant endemic to the mountains of southern Europe
and ‘Turkey, is resolved as sister to the other taxa
in the ITS and combined trees (Figs. 1, 2, 5, 6) but
collapses in a polytomy with other lineages in the
chloroplast-based tree (Fig. 3). The remaining Au-
laxyper lineages correspond to polyploid taxa of the
Festuca rubra complex. Hexaploid representatives
of this group collapse in a polytomy with a clade
of high polyploids; these taxa include two grassland
species, the typical Euro-Siberian Festuca rubra,
and the western Mediterranean Festuca iberica. The
high polyploidy clade is formed by the octoploids

Volume 91, Number 1
2004

Torrecilla et a 149

Phylogenetic Relationships of Vulpia

Festuca juncifolia and E rothmaleri and the deca-
ploid Festuca nevadensis. These are robust taxa en-
demic to territories of western Europe and northern
Africa. The octoploid taxon F rothmalert accounts
for the highest nucleotide substitution rates found
within the FEVRE perennials in both ITS and trn L-
F sequences as reflected in its long branches in the
Bayesian trees (Figs. 2 and 4). Optimal minimum
folding energies and estimated structures of the
RNA transcript are similar to those of other Festuca
taxa. The elevated rates of variability detected in
the ITS region of these perennial polyploids are in
(2000)
who recorded higher levels of ITS diversity in sev-

agreement with the findings of Саш et al.

eral polyploid taxa of Festuca subg. Schedonorus
and of Festuca sect. Aulaxyper than in their diploid
relatives. The rapid rate of evolution shown by this
perennial group of polyploid red fescues can be
likely associated to their putative recent hybrid or-
igin (Kerguélen & Plonka. 1989).
FESTUCA SECT. FESTUCA AND WANGENHEIMIA

Another circumscribed group of taxa of the
combined ITS and trn L-F trees is that correspond-
ing lo the Festuca group. which shows total boot-
strap support (Fig. 5). This clade is recovered
the two separate ITS and trn L-F analyses with rel-
atively high bootstrap and posterior. probability
support, but the relationships among the taxa are
unresolved in most cases (Figs. 1—4). Similar lack
of resolution is observed in the consensus tree de-
picted in Figure 5 except for the sister relation-
ship of Festuca frigida to the remaining taxa. The
Festuca lineage shows an intermediate rate of nu-
cleotide substitution among the perennial FEV RE
groups, which is lower if compared to those of the
annual ones. However, E frigida (diploid). a tiny
restricted endemic plant from Sierra Nevada
(southern Spain). presents the highest mutation
The

higher substitution rate of this taxon might be re-

rates within the studied “ovina” fescues.

flected in its sister placement in the ITS and com-
L4. 0, OF

gonensis (tetraploid) and E indigesta (hexaploid),

bined trees (Figs. Inclusion of V. ara-
the only polyploid representatives of this group
sampled in the study, in the analyses did not alter
the topologies of the diploid-based trees (results
not shown). The relationships between these poly-
ploid species with respect to their potential dip-
loid relatives could not be established firmly due
to the overall lack of resolution of the clade and
to the present shortage in taxon sampling for this
largest group of predominantly holarctic Festuca
1986).

taxa (Ainscough et al.. However, some in-

sights about taxonomic and biogeographical rela-
tionships among the studied taxa could be spec-
recovered in the
3. 4).

clade shows a polytomy of the Euro-Siberian-bo-

ulated on from the clades

chloroplast trnL-F tree (Figs. The Festuca
real terminal taxon Festuca ovina (diploid), an un-
resolved western Mediterranean mountain clade
formed by E frigida and the close vicariant dip-
loid taxa H alpina and F. glacialis, and a polytom-
ic clade of Mediterranean steppe orophytes Fes-
tuca hystrix (diploid) and three members of the К
(Saint-Yves. 1925: Markgraf-
Dannenberg, 1985), hexaploid E indigesta and the

indigesta complex

sister taxa FL longiauriculata (diploid) + К. ara-
gonensis (tetraploid). Two other studied taxa that

have been conventionally classified within the
Festuca section (E plicata and F clementet)
(Markgraf-Dannenberg, 1980; Fuente & Ortuñez.
1998) fall apart from this clade. Both species bear
distinctive morphologic al traits that separate them
from the typical “ovina” fescues and show sub-
stantial differences in their respective substitution
rates. The odd resolution of these Festuca taxa
may indicate that the broad Festuca sect. Festuca
taxon. as presently circumscribed, may be an ar-
tificial assemblage of different lineages in need of
deeper investigation. Our resolved Festuca lineage
includes the type species and other consectional
taxa that share most of the distinctive morpholog-
ical traits of the

Wangenheimia is resolved as sister to the Fes-

“ovina” group.

tuca clade in the combined ITS and trnl.-F trees

(Figs. 5 and 6) and in the separate trnL-F topolo-
vies (Figs. 3 and 4). both with relatively high boot-
strap and posterior percentage support. However,
this taxon is linked to Vulpia unilateralis in the
ITS-based trees

of Wangenheimia are similar to those of the other

(Figs. 1 and 2). Substitution rates
annual lineages but higher than the Festuca ones.
However. Wangenheimia shares with the “ovina”
group several nucleotide synapomorphies and a 5
bp indel in the trn L-F. region: exclusion of this gap
character did not alter the topology of the clade.
which also showed relatively high support indicat-
ing that Wangenheimia could have acquired its
chloroplast genome from an ancestral Festuca do-
nor. Wangenheimia shows few morphological affin-
ities with the Festuca taxa but more with the Vulpia
ones. However. Wangenheimia is distinguished
from Vulpia and resembles Festuca sect. Festuca in
its two subequal glumes and unawned lemmas. This
taxon is distributed in xeric continental areas of the

western Mediterranean region,

150

Annals of the
Missouri Botanical Garden

VULPIA SECT, VULPIA P.P. (POLYPLOID) AND PSILURUS
The clade Psilurus + polyploid Vulpia (Vulpia
sect. Vulpia p.p.) shows one of the highest bootstrap
values within the core FEVRE groups (Fig. 5). The
common ancestry of tetraploids Psilurus incurvus
and Vulpia ciliata and hexaploid Vulpia myuros is
recovered in both the ITS tree (Fig. 1) and the trnL-
F tree (Fig. 3), though the phylogenetic relation-
ы of this polyploid lineage to other dcn
FEVRE relatives have not been yet resolved. '
Bayesian 5096 majority-rule consensus tree o
the Psilurus + polyploid Vulpia group nested in an
unresolved clade that also includes the Aulaxyper
* diploid Vulpia lineage and their allies in a sep-
arate subclade (Fig. 6). The expected close relat-
edness of the polyploid Vulpia sect. Vulpia taxa to
the other consectional diploid taxa (Cotton & Stace,
1977; Stace, 1981) has not been confirmed by the
present data. Representatives of the two polyploid
species intermix in a clade sister to Psilurus in the
ITS and ITS/trnL-F based trees (Figs. 1. 2, 5. 6).
though they collapse with Psilurus in a polytomy in
the trnL-F based trees (Figs. 3, 4). The close re-
latedness of Vulpia ciliata and Vulpia myuros is
mostly based on the ITS characters (Figs. 1, 2
Substitution rates of the Psilurus + polyploid Vul-
pia lineage are roughly similar to those of the dip-
loid Vulpia lineage for both ITS and trnl.-F se-

quences; however, the two groups show the lowest

—

substitution rates of all Vudpia taxa indicating a
likely slower evolutionary pace. Differences are es-
pecially noticeable with respect to the highly het-
erogeneous sequences of the Loretia assemblage.
The relatedness of Vulpia ciliata and V. myuros
is congruent with some of their shared morpholog-
ical attributes, otherwise characteristic of the typi-
cal section Vulpia (Cotton & Stace, 1977); however.
the link of these two taxa to Psilurus is more un-
expected. Hexaploid Vulpia myuros is the type spe-
cies of the genus; this taxon strongly resembles dip-
loids Vulpis muralis and V.

bromoides in gross
morphology, although our molecular data do not
support a close phylogenetic relationship. Vulpia
ciliata and Psilurus share a 3-veined lemma, a 1-
veined upper glume, and swollen epidermal cells.
Vulpia ciliata bears other unusual traits that are not
present in typical section Vulpia, such as spikelets
with large distal sterile florets and a hyaline margin
of the upper glume (Paunero, 1964; Cotton & Stace,

71). Psilurus has been considered to be close to
section Apalochloa in Vulpia (V. unilateralis) based
on several morphological and anatomical characters
(Vignal, 1979); however. placement of the latter
taxon is rather ambiguous (Figs.

L

VULPIA SECTS, SPIRACHNE, MONACHNE, LORETIA,
APALOCHLOA, CUTANDIA, FESTUCA PLICATA, AND
CTENOPSIS

AND

A monophyletic group resolved by the combined
ITS and trnL-F analysis is that of the sections Spi-
rachne, Monachne, Loretia, and Apalochloa of Vul-
pia plus Cutandia maritima, Festuca plicata, and
Ctenopsis delicatula (Figs. 5 and 6). Representa-
tives of three sections of Vulpia (sects. Spirachne,
Monachne, Loretia), Cutandia maritima, and Fes-
tuca plicata are distinctly resolved in a moderately
supported clade, whereas those of Vulpia sect.
Apalochloa and Ctenopsis link in a clade sister to
the former clade though none of these relationships
is supported (Fig. 5). The monophyly of the first
group is mostly based on ITS data (Figs. 1, 2),
whereas the link of these two lineages with those
of representatives of Festuca sect. Exaratae plus E
pyrenaica and Е clementei is recovered by the trn L-
F characters (Fig. 3). Deletion of one 4 bp trnL-F
indel from the analysis provokes the disarticulation
of this group, except for the two single subclades
supported by nucleotide characters in the parsi-
mony-based tree (Fig. 3); nonetheless, the mono-
phyly of the Spirachne + Monachne + Loretia +
Cutandia + F. plicata assemblage is recovered with
relative high support in the Bayesian tree (Fig. 4),
which is only based on sequence data.

Sections Monachne and Loretia intermix in the
two separate subclades recovered by the ITS data
(Figs. 1, 2) and in the combined trees (Figs. 5, 6).
Vulpia brevis, the single taxon of section Spirachne,
is resolved as the closest relative of Vulpia fasci-
culata, the type species of section Monachne (Figs.
э, б), a relationship mostly based on the ITS
acters (Figs. 1, 2).

char-
The two sister taxa (Vulpia brevis
+ V. fasciculata) share a number of structural char-
acters, like a cleistogamous breeding system, spike-
lets with an apical group of sterile florets, awned
upper glume, and distally dilated pedicels, that
were postulated by Cotton and Stace (1977) as ev-
idences of their close taxonomic relatedness. Vulpia
sicula is the next closest relative of the Vulpia brev-
is + V. fasciculata pair (Figs. 1, 2, 5, 6). The taxon
shows a chasmogamous breeding system and full
fertile flowered spikelets, characters that are typical
of Vulpia sect. Loretia; most noticeably, Vulpia si-
cula is a perennial caespitose species that can hy-
bridize with Festuca rubra in experimental crosses
though not spontaneously (Barker & Stace, 1982).
Based on morphological, karyological, and repro-
ductive characters Stace and Cotton (1973) consid-
ered Vulpia sicula to be related to other Vulpia sect.
Loretia taxa. Our ITS data indicate that Vulpia si-

Volume 91, Number 1
2004

Torrecilla et 151

al.
Phylogenetic Relationships of Vulpia

cula is most likely a close relative of Vulpia species

of sections Spirachne, Monachne (V. fasciculata

herein). and Loretia (V. geniculata herein) (Figs. 1

2. 5. 6) though the cpDNA data point toward some
unsupported affinity of V. sicula to V. unilateralis
(Figs. 3 and 4). Vulpia geniculata. another repre-
sentative of section Loretta that bears large repro-
ductive organs, is also nested in this clade and re-
solved as sister to the previous group.

The resolution of the second group of Vulpia taxa
((Vulpia membranacea + V. fontqueriana), (Vulpia
alopecuros + Cutandia)) is highly supported in
both the combined and the ITS-based topologies
(Figs. 1. 2. 5. О); the sister relationships of Vulpia
alopecuros and Cutandia maritima are also recov-
ered in the ul tree (Figs. 3. 4). Vulpia mem-
branacea and V. fontqueriana are very similar mor-
phologically: Y. fontquertana was described from
southern Spain by Melderis and Stace (1968) based
on its single fertile floret. per spikelet and long

pointed lemma callus. These two diploid represen-

—

allves of jan sect. Monachne show the typical
characters of this group (cle ier breeding
system, reduced number of fertile flowers per

spikelet). but they do not link together with the type
species (V. fasciculata) in the ITS-based tree (Figs.
1. 2). Inclusion of tetraploid V. fasciculata in the
diploid data set analysis resolved it as sister to dip-
loid V brevis but not to their consectional taxa. By
contrast, the Bayesian frnL-F analysis resolves V.
fasciculata as sister to a consectional low-supported
V. membranacea + V. fontqueriana clade and links
V. brevis to the V. alopecuros + Cutandia maritima
clade (Fig. 4). Because all representatives of Vulpia
sects. Monachne and Spirachne (monotypic) have
been sampled in the present study, the monophyly
of section Monachne is disputed by the more abun-
dant ITS characters (Figs. J. 2. 5. 6) but not by the
trnl.-F ones (Fig. 4). The tetraploid taxon V. fasci-
culata is likely of hybrid origin (Monachne X Spi-
rachne). having inherited its chloroplast’ genome
from a Monachne ancestor. The resolved patterns
are in general agreement with classical circum-
scriptions of these groups and have provided an
evolutionary framework to explain the origin of tet-
raploid V. fasciculata.
Resolution of the clade V. alopecuros + Cutan-
dia maritima is recovered by both ITS and trnl.-F
data with high bootstrap and posterior. probability
support (Figs. 1—1) and is therefore reflected in the
combined trees (Figs. 5. 6). However, the close re-
latedness shown by Cutandia maritima to this Vul-
pia group is mostly unexpected. Stace (1978b) sug-

gested a close taxonomic affinity of Cutandia to
Desmazeria, whereas Soreng and Davis (2000)

found Cutandia (С. memphytica) to be nested with-
in their “Parapholiinae” clade in a grade of Sphen-
opus (Cutandia (Catapodium (Desmazeria (Hainar-
dia + f
Cutandia maritima to V. alopecuros is based on sev-
trnL-F
characters being the only group of the clade that is

The sister relationship «

Parapholis)))).

eral synapomorphic ITS and nucleotide

ч

not disassembled when the trnL-F indels are ex-

cluded from analysis (results not shown). The ex-
tremely high substitution rate showed by C. mari-
tima in its ITS region, reflected by the length of its
branch in the Bayesian-based tree (Fig. 2), was cor-
related with its low % G + C content and the high
minimum-free folding energies of its ITS] RNA
transcript, though those values were not dramati-
cally different from the ones estimated for other
ingroup and outgroup taxa. These results suggest
that the IT

putative pseudogene or just a highly variable one.

S sequence of C. maritima could be a

The distorting effects caused by paralogous ITS

copies in phylogenetic reconstruction have been
manifested in different analyses of angiosperms
(Buckler et al., 1997: Mayol & Rosselló, 2001).

Phylogenies potentially affected by ITS pseudo-
genes have also been reported in Lolium (Саш et
al.. 2000). i

a spurious phylogeny, the ITS analyses were recon-

In order to avoid the risk of recovering

ducted deleting Cutandia maritima from the data
set. The parsimony and Bayesian trees showed the
same topology and similar levels of branch support
to the ones depicted in Figures J and 2 (results not
shown). indicating that the exclusion of this species
does not alter the relationships recovered for the
remaining taxa. E
provided by the ITS data. the trnL-F data still re-
. alopecuros and С.

Even leaving out the information

cover a sister relationship for |
maritima. the only well-supported clade of this
group (Figs. 3. 4). Cutandia maritima shows an in-
termediate rate of substitution in this chloroplast
genome region, not significantly higher than that of
V. alopecuros and similar to those of other Vulpia
sect. Loretia taxa (results not shown). Therefore, the
relationships presented here between C. maritima
and V. alopecuros are strongly supported by trnL-F
data. A
tandia will be necessary in order to establish its

arger sampling of representatives of Cu-

Mhvlogenetic relationships within the festucoids
pnyiog |

and other related lineages and to determine if this

axon is a natural genus. The placement of Vulpia
alopecuros in the clade is congruent with its taxo-
nomic affinities: this taxon bears the general attri-
butes of section Loretia but presents a glabrous ova-

ry apex. pointed elongated callus. and a minute
l-veined lower glume (Cotton & Stace, 1977).
Barker and Stace (1984, 1986) indicated the ex-

152

Annals of the
Missouri Botanical Garden

treme genetic isolation of Vulpia alopecuros from
other Vulpia taxa and suggested a distinct sectional
treatment for it. Our results resolve V. alopecuros as
the sister taxon of the V. membranacea + V. fo-
ntqueriana clade

Festuca plicata, a taxon classified within Festuca
sect. Festuca, shows an unexpected relatedness to
this Spirachne + Monachne + Loretia + Cutandia
group (Figs. 5, 6) that is confirmed by the two sep-
arate ITS and trnL-F based analyses (Figs. 1
Diploid Festuca plicata is an endemic Ibero-Mah-
grebian taxon characterized by several uncommon
Festuca ovina traits; it resembles Vulpia in its long-
awned lemma. Festuca plicata was recently includ-
ed in Festuca sect. Festuca by Fuente and Ortufiez
(1998); our combined ITS and trnL-F analysis dem-
onstrates that Festuca plicata is not related to the
studied
laxa.

"ovina" group but to this clade of Vulpia

Vulpia unilateralis, the single representative of
Vulpia sect. Apalochloa is recovered as the sister
taxon of Ctenopsis in the combined trees depicted
in Figures 5 and 6; however, its phylogenetic place-
ment is not satisfactorily resolved in any of the in-
dependent ITS and trnL-F analyses (Figs. 1—4).
Vulpia unilateralis is shown to be related to Wan-
genheimia, Narduroides, and Ctenopsis in the ITS
Bayesian tree (Fig. 2) but is nested within the Spi-
rachne + Monachne + Loretia clade in the trn L-F
Bayesian tree (Fig. 4), though none of those rela-
tionships is well supported. The distinctness of sec-
tion Apalochloa from other sections of the genus
Vulpia is corroborated by several characters; Vulpia
unilateralis bears a single-borne spikelet per node,
shortly awned lemma, and several anatomical pat-
terns in vegetative and floral epidermises that link
it to Psilurus (Vignal, 1979). Despite the apparent
similarities between these two taxa, our results in-
dicate that Vulpia unilateralis and Psilurus incurvus
belong to different phylogenetic lineages of the
FEVRE group.

Ctenopsis delicatula is a close relative of this Spi-
rachne + Monachne + Loretia + Cutandia + Fes-
tuca plicata group. This annual taxon shows a sister
relationship to Vulpia geniculata in the trnL-F
Bayesian tree (Fig. 4) but is otherwise unresolved
within the FEVRE clade in the ITS parsimony
(Fig. 1). The combined ITS and
` analysis recovers a siste

based topology
trnL- r relationship of
Ctenopsis delicatula to Vulpia ies favored
by the ITS characters. Ctenopsis has been frequent-
ly classified within Vulpia based on their strongly
unequal glumes and some other floral traits (Clay-
ton & Renvoize, 1986) but is distinguished from it
by its rigid panicle, and a caryopsis free from the

palea with a short hilum (Paunero, 1963; Cotton &
Stace, )

Representatives of the four sections Monachne,
Spirachne, Loretia, and Apalochloa of Vulpia form
a distinct though paraphyletic assemblage within
the FEVRE group; Cutandia maritima, Festuca pli-
cata, and Ctenopsis delicatula are nested within it.
This Р shows the highest substitution rates of
all studie "VRE lineages for both genomes,
though thes are more pronounced in the ITS region
(even when С. maritima is excluded from analyses),
thus raising contention about the loss of deep phy-
logenetic signal in the highly heterogeneous taxa
and the potential influences that long-branch at-
traction and site saturation might have inflicted on
these phylogenies. Despite the potential risk of
some artifactual relationships caused by an excess
of homoplasy, the evolutionary framework depicted
зеге shows a close relationship for most of the Vul-
pia lineages, which likely form a paraphyletic
group recently derived from a common ancestor. On
the other hand, the separate placements shown by
representatives of the typical Vulpia sect. Vulpia
clearly demonstrate the polyphyly of this genus.

FESTUCA SUBSECT.
PYRENAICA

EXARATAE, Е CLEMENTEI, E

Some unresolved taxa of the core FEVRE group
are those belonging to Festuca subsect. Exaratae
(Festuca borderei, F. capillifolia) plus Festuca cle-
mentei and H. pyrenaica. These taxa form a para-
phyletic basal lineage to the Spirachne + Monach-
ne + Loretia + Apalochloa + Cutandia + F.
plicata + Ctenopsis clade in the combined parsi-
mony-based ITS and trnL-F tree (Fig. 5) where the
four of them collapse in a polytomy with the clade
of Vulpia taxa and its allies. This topological posi-
tion is mostly coincident with that of the trnL-F
parsimony-based tree (Fig. 3), though neither it nor
the one in Figure 5 is supported. The link between
these four taxa and the Vulpia clade is based in one
trnL-F 4 bp indel; the Bayesian analysis, which
includes only nucleotide characters, shows a basal
unresolved position of this Exaratae group of taxa
with respect to the more recently evolved FEVRE
lineages in the trnL-F and combined trees (Figs. 4
and 6 ,
The Exaratae group was first circumscribed
based on the possession of invaginate leaf sheaths
(Saint-Yves,
with intravaginal versus extravaginal and intravag-
inal shoots (Saint-Yves, 1922; Maire, 1955; Mark-
graf-Dannenberg, 1985) that otherwise link them,
respectively, to the Festuca and Aulaxyper groups

1922); this taxon includes a variety

Volume 91, Number 1
04

Torrecilla et al. 153

Phylogenetic Relationships of Vulpia

to which they have been frequently misattributed.
Our two studied representatives of Festuca subsect.
Exaratae and the F clementei and H. pyrenaica taxa
are narrow endemics of the western Mediterranean
area, and each of them shows singular morpholog-
ical traits. However, none is closely related to the
core group of fine-leaved fescues, as demonstrated
in the ITS 5. 6).
The basal position recovered for these lineages in

and trnL-F based topologies (Figs.

the Bayesian trees is in agreement with the low
substitution rates detected in their chloroplast: ge-

nome, which are significantly slower than those of

the Aulaxyper, Festuca, and the annuals groups.
Our preliminary results indicate that Exaratae s.l.
(incl. Festuca clementei and F pyrenaica) could
represent older evolutionary lineages than those of
the Festuca ovina and the Е rubra s.l. groups.

VARDUROIDES AND MICROPYRUM

An additional problem is manifested by the con-
trary placement of the genera Micropyrum and Nar-
duroides that distantly attach to different lineages
of the FEVRE clade on nuclear- and chloroplast-
1—4).

more closely related to Apalochloa. Wangenheimia,

based reconstructions (Figs. Narduroides is
and Ctenopsis in the Bayesian ITS based tree (Fig.

2) but is sister to the F ovina and E rubra clade
in both parsimony and Bayesian trnl.-F based trees
(Figs. 3, 4). Conversely, the Micropyrum clade is
unexpectly resolved as sister to the F rubra group
in the ITS based trees (Figs.
the Psilurus + polyploid Vulpia clade in the trnl.-

1. 2) but as sister to

F based trees (Figs. 3, 4). However, none of these
relationships is well supported in any case. The two
Micropyrum taxa included in this study ar
M. patens) link together in highly
14).

tution rates shown by the Micropyrum and Nardu-

rum tenellum,
supported generic clades (Figs. The substi-
roides lineages are similar to those found for the
other ephemeral taxa except for the low rate of the
Narduroides ITS region. This suggests that the dis-
tinct phylogenetic relationships recovered for each
lineage might be influenced by different homopla-
sious changes. Alternatively, Micropyrum and Nar-
duroides could be genera of hybrid origin with dif-
respective

ferently inherited. genomes. from. their

ancestors. None of these hypotheses can be re-
solved with the present data. Narduroides, a mono-
typic genus characterized by its subequal glumes,
chartaceous to coriaceous lemmas, and a caryopsis
slightly adherent to palea, with a punctiform hilum
(Stace,
Vulpia—Desmazeria complex by Stace (1981

1978a) was considered to be related to the
but
was Classified within tribe Hainardieae by Clayton

—

and Renvoize (1986). Our phylogenetic results in-
dicate that Narduroides may be a recently evolved
taxon of the core FEVRE clade.

SUMMARY. HYBRIDIZATION, POLYPLOIDY, AND
LIFE-CYCLE STRATEGIES AS THE MAIN DRIVING
FORCES IN THE EVOLUTIONARY HISTORY OF THE
FEVRE LINEAGES

The phylogenetic hypothesis recovered from the
present study supports the four resolved lineages
Aulaxyper + diploid Vulpia, Festuca + Wangen-
heimia, Psilurus + polyploid Vulpia, and Spirachne
+ Monachne + Loretia + Apalochloa + Cutandia
+ E plicata + Ctenopsis within the FEVRE group
after the separate and simultaneous analysis of the
nuclear ITS and the chloroplast trnL-F regions. The
first three lineages and two clades of the last group
(Spirachne + V. fasciculata + Loretia and V. mem-
branacea + V. fontqueriana + V. alopecuros + Cu-
tandia) show strong to moderate bootstrap and pos-
terior probabilities supports. A likely hypothesis of
evolution for most of the studied taxa is presented
in the trees depicted in Figures 5 and 6. Nonethe-
less, the phylogenetic relationships among these
main groups still remain obscure: internal resolu-
tion of the deep branches of the FEVRE group has
not been achieved with the present data set indi-
cating that the failure of the sequenced regions to
resolve the early divergences of this group of grass-
es could be associated with events related to line-
age sorting, hybridization, and polyploidization, re-
current phenomena which are otherwise common in
the grass family (Kellogg et al., 1996; Davis & So-
1993: Soreng & Davis, 2000). The strong dif-

ferences observed in the substitution rates among

reng.

different lineages could also increase instances of
homoplasy for the rapidly evolving taxa and might
affect phylogenetic analysis with undesirable. ef-
fects like long-branch attraction and site saturation
(Hillis, 1998: Wendel & Doyle, 1998; Саш, 1998).
Despite potential cases of artifactual reconstruction
for some rapidly evolving FEVRE groups, the con-
current. phylogenetic resolution and the similar
rates of substitutions obtained for the main FEVRE
lineages indicate that the recovered topologies like-
ly reflect their true evolutionary relationships.
Compelling evidences have demonstrated the
key role played by hybridization in the speciation
of the pooid grasses where both intergeneric and
intrageneric taxa have been documented for several
tribal lineages (Soreng & Davis, 2000, and refer-
ences therein). Recurrent hybridization followed by
polyploidy is a common phenomenon within the

“fine-leaved” Festuca as demonstrated for most of

154

Annals of the
Missouri Botanical Garden

the Festuca sect. Aulaxyper taxa, which are consid-
ered hybrid-swarms of putatively recent origin
(Ainscough et al., 1986). Introgressive hybridiza-
tion and polyploidization constitute major driving
evolutionary forces within the angiosperms (Steb-
bins, 1950, 1956; Brochmann et al., 1992; Soltis
et al., 1995; Cook et al., 1998; Soltis & Soltis,
1999) where recurrent origins of polyploid species
seem to be the rule rather than the exception. How-
ever, while multiple origins of recently formed poly-
ploid taxa could be traced with confidence using
СИ (pes ular markers (Soltis et al., 1995;

Cook e 998). appalling conflicts arise in the
быш d d reticulation events where parental
lineages may have become extinct or where hybrid

—
—

derivatives show closer morphological and genomic
affinities to one of the parental taxa. Well-docu-
mented cases have been presented for most inter-
generic X Festulpia taxa that have gained the mor-
phological attributes of the red fescue parent, which
performed successfully as the pollen donor, show-
ing their ability for repeated backcrossing with that
parent but not with the female Vulpia one (Barker
& Stace, 1984; Ainscough et al., 1986). Artificial
crosses and derivative backcrosses that mirror the
spontaneous hybridizations followed by these plants
in the wild are clear examples of the difficulties of
tracing back the identity of the original parental
lineages in this highly introgressed FEVRE group.

Efforts to unravel the reticulation events postu-
lated in this group of grasses have failed for some
diploid lineages (i.e., Narduroides, Micropyrum) as
well as for the polyploid Psilurus + Vulpia clade.
Conflicting topologies from differently inherited ge-
nomes have been reported in the tribe Triticeae
(Kellogg et al., 1996; Mason-Gamer & Kellogg.
1997), where organellar and nuclear data sets re-
cover different histories of diploid genomes. Chlo-
roplast-based phylogenies have been considered a
safer way to recover the underlying evolutionary
trends of highly reticulate groups, like in the Pooi-
deae (Soreng & Davis, 2000), potentially avoiding
the risks presented by recombinant nuclear char-
acters and by admixed polyploid genomes. How-
ever, plastid data have led to incorrect pictures of
evolutionary history in some angiosperm
where more rapidly evolving nuclear genes
satisfactorily recovered the relationships at the
deep internal branches of the trees (Cronn et al.,
2002). In the FEVRE group, the more highly var-

groups
ave

iable ITS region has proven to be the source of

major informativeness though it is mostly concor-
Ad-

ditive polymorphisms, changes in concerted evo-

dant with that retrieved from the chloroplast.

lution of the ITS region toward one of the parental

ribotypes, and recombinations may have also oc-
curred in different lineages of the FEVRE group as
these operate in highly reticulate
groups (Fuertes-Aguilar et al., 1999; Whitall et al.,
2000). Such events could pass unobserved or be
untraceable in extant organisms of recurrently in-

mechanisms

trogressed groups, thus making more difficult the
reconstruction of the past history of some lineages.

Ongoing in situ hybridization between different
Vulpia species and the red fescues (F rubra group)
has been reported for representatives of Vulpia sect.
Vulpia (Vulpia myuros, V. bromoides) and Festuca
sect. Aulaxyper (Festuca rubra, F. nigrescens) (Ain-
scough et al., 1986) and of Vulpia sect. Monachne
(Vulpia fasciculata) and Festuca sect. Aulaxyper
Festuca rubra, F. juncifolia) (Stace & Cotton,
1974). These spontaneous crosses have been inter-
preted as indicators of the close genetic relation-
ships between the respective parental groups (Ain-
scough et al., 1986). The genetic affinities claimed
for them are in close though not complete agree-
The close re-

—

ment with our phylogenetic results.
ationship recovered for the diploid representative
of Vulpia sect. Vulpia (Vulpia bromoides) and Fes-
tuca rubra is in contrast with the lack of apparent
evolutionary links between polyploid representa-
tives of Vulpia sect. Vulpia (hexaploid Vulpia myu-
ros) and of section Monachne (tetraploid Vulpia fas-
ciculata), which intercross more frequently with
hexaploid and octoploid taxa of the Festuca rubra
complex in the wild. These contradictions also ex-

—

tend to the disparate placements found for the dip-
loid and polyploid Vulpia sect. Vulpia lineages
within the FEVRE group. Assortative matching and
recurrent polyploid formation, common phenomena
in several groups of angiosperms (Soltis & Soltis,
1993), could have been the hidden mechanisms be-
hind the multiple origins of these diverging Vulpia
polyploids. Recently derived polyploid taxa, like
those of the Psilurus + polyploid Vulpia clade,
might have arisen at different evolutionary times.
Although the identity of their potential genome do-
nors has not been established yet, the close geno-
mic affinities shown to the red fescues in present
spontaneous intergeneric crosses and the morpho-
logical similarity of some of them (tetraploid and
hexaploid Vudpia taxa) to consectional diploid taxa
points toward the contribution of the Aulaxyper +
diploid Vulpia lineage in their origin.

Substitution rates might also be indicative of dif-
ferent selection mechanisms that operate in the
speciation process (Gaut et al., 1996; Barraclough
et al., 1996; Barraclough & $ ee. 2001; Job-
son & Albert, 2002; Zhong et al., 2002). Relative
rate tests conducted within the FEVRE group have

Volume 91, Number 1
2004

Torrecilla et a 155

l.
Phylogenetic Relationships of Vulpia

detected a general evolutionary pattern where old
perennial lineages evolve significantly slower than
the recently derived annual ones, suggesting the
presence of some stabilizing selection acting on the
perennial taxa in contrast to a rapid adaptive spe-
ciation of the ephemeral taxa. The multiple arrays
of morphological and reproductive traits manifested
by the FEVRE ephemeral taxa that moved taxon-
omists to classify them in different genera can be
interpreted as the Consequence of selection release
resulting in rapid, pulse-like diversification events.
In this respect. our findings support the speciation
rate hypothesis that connects increased nucleotide
substitution with increased taxonomic diversifica-
1996; Barraclough & Sa-
volainen, 2001). Although the acquisition of the an-

tion (Barraclough et al..

nual life-cycle habit has presumably fostered the
speciation rate of the ephemeral FEVRE taxa. other
perennial lineages with relatively high rates of nu-
cleotide substitutions but longer generation times
(Le... Festuca sect. Aulaxyper) may have also ex-
perienced an increased rate of cladogenesis. Tor-
recilla et al. (2003, and unpublished data) have
recently found that some Macaronesian and Amer-
ican Festuca taxa currently attributed to different
fescues (i.e.. sect.

groups of the “broad-leaved”

Amphigenes, sect. Subulatae) are close relatives of

the red fescues. The higher mutation rates shown
by the Au/axyper taxa compared to those of the oth-
er perennials might have resulted from diverse re-
current introgressions with other festucoid lineages
increasing the genetic pool of this hybrid complex.
An evident evolutionary trend toward a short an-
nual life-cycle and a reduction in habit and repro-
ductive size has probably evolved several times
within the FEVRE group as manifested in the Spi-
rachne + Monachne + Loretia + Apalochloa
Cutandia + F. plicata + Ctenopsis lineage. By con-
trast. a progressive increase in size and robustness
has been developed in the more recently evolved
perennial complexes of the F rubra group that are
mostly formed by vigorous hybrid taxa that also
propagale vegetatively. These apparently opposite
life cycle and reproductive strategies coupled
each case with recurrent. hybridization and poly-
ploidy have been major factors that likely triggered
the speciation processes within the separate line-
ages of the FEVRE group at different evolutionary
times. The effects of selection processes focused on
large mosaics of populations covering rapidly ex-
panding broad geographic ranges after the glacia-
tions, like those experienced by the successful
polyploid and clonally propagating red fescues,
must differ from those experienced by narrow en-
demic relictual species, like most of the annual and

some of the oldest perennial FEVRE lineages. The
evolutionary scenarios depicted here for the
ephemeral and highly introgressed perennial line-
ages of the fine-leaved Festuca should be examined
across other festucoid lineages where evolutionary
trends toward short-life cycle perennial poly-
ploid-vigor have evolved independently in several
lineages. Biogeographical patterns of most of the
ephemeral FEVRE groups covered in the present
survey indicate that these annual lineages likely
radiated in the Mediterranean region, the area in
which the potential diploid ancestors are endemics.
An evolutionary hypothesis about an early diver-
gence of most of the FEVRE diploid annual line-
Vulpia p.p..

ages (Vulpia sect. Micropyrum. Nar-

duroides, Wangenheimia) and of a secondary
radiation of the highly polyploid complexes (Fes-

are also

—

tuca sects. Aulaxyper and Festuca p.p.

supported by our phylogenies. A larger and more
resolved framework should be constructed for the
FEVRE

speciation of these grasses.

lineages in order to estimate the date of

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=.
=

GEOGRAPHICAL
DIVERSIFICATION OF
TRIBES EPILOBIEAE,
GONGYLOCARPEAE, AND
ONAGREAE (ONAGRACEAE)
IN NORTH AMERICA, BASED
ON PARSIMONY ANALYSIS
OF ENDEMICITY AND TRACK
COMPATIBILITY ANALYSIS:

Liliana Katinas,? Jorge V. Crisci.? Warren

L. Wagner,* and Peter C. Hoch'

ABSTRACT

Tribes Epilobieae, Gongyloe arpeae, and Onagreae. a monophyletic branch in the family Onagraceae,

Madrean Floristic

endemic to or having their i major basal radiation in the

con pesi genera

Region of southwestern North America.

Parsimony analysis of endemicity (PAE) and o (track compatibility analysis) were pe 1 in rodir to

seek an historical explanation for the patterns of hig
li

one areas of endemism are delimite

suggest a close re Sonet of eastern and western North A

to the Palearctic. i

that differs from those of the Holarctic. '
side of North America, with the spe
Key words:

track s

diversity and endemicity for the group in this region. Tw
‚ based on previous biogeographic

T3 species, a strict consensus

xican
vo strongly supported generalized tracks: one
orth America. " AE and panbiogeographical analyses of the ФА ршн] patterns

ik assoc lation be tween 1 northe п North. America and Asia.

E
biogeography, endemicity, Madrean, Onagraceae,

enty-
schemes and presence of endemic plant and
AE cladogram shows four main groups

eas, western North America, and eastern North America. Track

includes eastern North America, and
of these taxa
America. with both areas more related to Е Neotropics than
The discovery of two tracks
al little re кй of North

panbioge каша 1

Recent developments in biogeography have
highlighted the importance of the spatial distribu-
tion of organisms as a direct subject of analysis
1999; Crisci, 2001; Crisci et al., 2000,
The Onagraceae, a moderate-sized. sharply

(Craw et al..
2003).
defined, homogeneous family, have been intensively
studied (Raven. 1979, 1988: Hoch et al., 1993:
2003, 2004) and thus constitute an

excellent group within which to develop such bio-

Levin et al.,

geographic studies.

The family Onagraceae includes six monogeneric

tribes—Circaeeae, Fuchsieae, Gongylocarpeae,

Hauveae. Jussiaeeae, and Lopezieae—and two

arger. more diverse tribes, Epilobieae and Ona-
1979: Hoch et al., 1993; Levin et al..

2003). Tribes Epilobieae, Gongylocarpeae, and On-

greae (Raven.
agreae, which form a monophyletic branch in the
family (Levin et al., 2003), are biogeographically
distinct because almost all 11 genera in these tribes
are endemic to or have had their major basal ra-

! The authors thank the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, ini: ee Missouri

Botanical Ga
came from the Smithsonian. [Institution
We also thank |

Andrew

systems program,

Mame eae. and for his encouragement of this project. We thank
for her great an кү in preparation of the figures and for logistic support for the project, and

in the figures. Denise Mix
Tom Hollowell for assistance with the A
anonymous reviewer for useful comments.

? División. Plantas л Мизео Ж!
museo.fenym.unlp.edu.ar, jerisci@netverk.c

La Sata,

rden, and Smithsonian mien T generous supp
ellon Fellowships in Structure and Evolution of Terrestrial Eco-
eter Raven Es selling the stage for this analysis through his long study of the
Map base map for the figures

Paseo del

t of this project; primary support for this project

Alice Tangerini for preparing the excellent graphic 5

. We also thank Matt Lavin, Jun Wen, and an

Bosque s/n, 1900 La Plata, Argentina. katinas@

ri
Department of Systematic Biology. in NL 166, Smithsonian Institution, P.O. Box 37012, Washington, D.C.

agner.warre n nmnh. Si.

P.O. Box 2

20013-7012, U.S.A. w
! Missouri Botanical Garden.

ANN. MISSOURI Bor.

90, Si. PS Missouri 63166-0299, U.S.A. peter.hoch@mobot.org.

GARD. 91: 159-185. 2004.

160

Annals
11 Eo Garden

diation in western North America. A primary con-
centration of genera exists in the Madrean Floristic
Region (Takhtajan, 1986), comprising the south-
western United States and northern Mexico. This is
an area of great geological and climatological com-
plexity with a rich and highly characteristic biota
не 1958; Axelrod & Raven, 1985; Takhta-
jan, |
Gongylocarpus,
Onagreae, and Xylonagra (Onagreae) are endemic
to western North America, and Camissonia, Clark-
ia, and Gayophytum (all Onagreae) have the great
majority of their taxa in the region, especially in
the California Floristic Province (Raven & Axelrod,
1978): each of the latter three genera also has one
or two species in temperate South America. The

until recently included in the

remaining genera of Onagreae (Calylophus, Gaura,
Oenothera, Stenosiphon) have centers of diversity
further east in North America, although Gaura ex-
tends into central Mexico and Oenothera into Cen-
tral and South America. One exception to the pre-
dominantly North American nature of these tribes
is Chamerion (the fireweeds), a genus of Epilobieae
with six of its eight species and one of two sections
endemic in Europe and Asia. Tribe Epilobieae def-
initely has a north temperate origin, with a distri-
bution pattern that suggests a more complex history
of diversification (Raven, 1976; Baum et al., 1994)
All seven sections of Epilobium (including the for-
mer segregate genera Boisduvalia and Zauschneria)
occur in or are restricted to the Madrean Region,
with the large section Epilobium diversified on all
other continents except Antarctica.

In order to seek the historical explanations that
led to the high diversity and endemicity of Epilo-
bieae, Gongylocarpeae, and Onagreae in Nort
America, we will analyze the patterns of distribu-
tion of species of these tribes native to North Amer-
ica (for a list of species and references, see Table
1). A focus on patterns of distribution requires con-
ceptual and methodological tools that allow com-
parisons to be made in a meaningful and informa-
tive way. Two modern approaches that allow this
kind of analysis are parsimony analysis of ende-

micity and track compatibility analysis (panbi-
ogeography) (Morrone & Crisci, 1990, 1995; Crisci

et al., 2000, 2003).

MATERIALS AND METHODS
AREAS OF ENDEMISM

An area of endemism is defined as an area of
nonrandom distributional congruence among differ-
ent taxa. It is identified by the congruent distri-

butional boundaries of two or more species, where

congruence does not demand complete agreement
on those limits at all possible scales of mapping,
but relatively extensive sympatry is a prerequisite
(Platnick, 1991)

Areas of endemism used in this analysis are de-
fined primarily by Takhtajan (1986) and Thorne
(1993) and validated by other biogeographical stud-
ies (i.e., Dice, 1943; Rzedowski, 1978; Brown et
al., 1979, 1998; McLaughlin, 1989, 1992; Ayala et
al., 1993; Escalante Pliego et al., 1993; Fa & Mo-
rales, 1993; Li & Adair, 1994; Liebherr, 1994a, b;
Morrone et al., 1999; Marshall & Liebherr, 2000;
Morrone, 2001). Because the focus of this study is
on a major plant lineage that has diversified in arid
North America, we have used small, closely defined
areas within the Madrean area. Some taxa within
this lineage have distributions that extend beyond
the North American regions. For these we used the
more broadly defined Neotropical, East Palearctic,
and West Palearctic regions, since they fall outside
of our area of focus in North America. Africa and
Australia were not included because native North
American species of these three tribes occur in
these areas only as exotics. Table 2 lists the areas
of endemism alphabetically, with taxa of the three
target tribes endemic to each area. Full descrip-
tions of each area of endemism, including sample
plant and animal taxa endemic to each, are provid-
ed in Appendix 1. The areas are illustrated in Fig-
ure 1

In some regions, the area delineations provided
by Hai (1986) and Thorne (1993) proved
somewhat vague or difficult to interpret, and in
those cases we used additional resources to deter-
For example, we used the
geographical subdivisions fund in The Jepson
Manual (Hickman, 1993) to more precisely delin-
eate the five regions in California (CAL, A,
MOJ, SON, and VAN; see Table 2 for area acro-
nyms). Similarly, we used the vegetational areas de-
scribed in Correll and Johnston (1970) to establish
the boundaries of the regions in Texas (APP, ATL,
CHI, NAP, and TAM). Additional sources used for
specific areas are referenced in the area descrip-
tion. In this way, distributional records could be
placed more precisely in the appropriate area of
endemicity.

mine the boundaries.

TAXA ANALYZED

The primary data for this analysis are the distri-
butions of 173 native species of Onagraceae tribes
Epilobieae, Gongylocarpeae, and Onagreae inhab-
iting North America (Canada, Mexico, United
States; Table 1). The distributional data were taken

Volume 91, Number 1 Katinas et al. 161
2004 Geographical Diversification

Table 1. List of species included in this analysis and source of distributional data (see text for details regarding
unpublished data). Gongylocarpus is listed here in tribe Onagreae; only recently (Levin et al., 2003) it was 1
to tribe ги arpeae. The number of each species corresponds with pate numbers in the data matrix (Table 3
Names of taxa are those currently in use. based on recent revisions. Two of the names, Oenothera deserticola and P
purpusit, cd have been re ied due to a nomenclatural e ramal 2004): Oenothera purpusil in the
sense used here will become O. deserticola, and the current O. deserticola will take a new name

Taxa Source of information

TRIBE ONAGREAE
Camissonia Link Raven (1962, 1969)

l. C. andina (Nutt.) P. Н. Raven

2. C. arenaria (A. Nelson) P. H. Raven

3. C. boothii (Douglas) P. H.

t. C. breviflora (Torr. & А. Gan р Н. Raven
5. С. brevipes (A. Gray) Р. Н. Raven

6. С. californica (Nutt. ex Torr. & A. Gray) Р. Н. Raven
7. С. campestris (Greene) Р. Н. Raven

8. Є cardiophylla (Torr.) P. Н. E

9. C. chamaenerioides (A. Gray) P. H. Hav
10. C cheiranthifolia (Hornem. ex Spreng.) fois
11. C. claviformis (Torr. & Frém.) P. H. Raven
12. C. confusa P. H. Rav
13. C. contorta (Douglas) тале
14. C. eastwoodiae (Munz) P. H. Raven
15. C. graciliflora (Hook. & Arn.) P. H. Raven

16. C. guadalupensis (S. Watson) P. Н. Raven
7. C. hilgardú (Greene) P. Н. Raven

18. C. hirtella (Greene) P. H. Raven

19. C. ignota (Jeps.) P. H. Raven

20. C. intermedia Р. Н

: aven
2]. C. kernensis (Munz) P. H. Raven

— +
—
d —

24. C. minor (A. Nelson) P. H. Raven
25. C. multijuga (S. Watson) P. H. Raven
26. C. ovata (Nutt. ex Torr. & А. Gray) P. Н. Raven
27. C. pallida (Abrams) P. H. Raven
28. C — (S. Watson) P. H. Raven
29. C. parvula (Nutt. ex Torr. & A. Gray) P. H. Raven
30. C. ee (S. Watson) P. H. Raven
31. C. pubens (S. Watson) P. Н. Raven
C. pusilla Р. Н. Rave

33. C. pygmaea (Douglas) P. H. Raven
34. C. refracta (S. Wa D P. H. Raven
35. C. robusta P. H. Rav
36. C. scapoidea (Torr. & A. Gray) P. H. Raven
37. C. strigulosa (Fisch. & C. A. Mey.) P. Н. Raven
38. C. subacaulis (Pursh) P. H. Raven
39. C. tanacetifolia (Torr. & A. Gray) P. H. Raven
40. C. walkeri (A. Nelson) P. H. Raven
Calylophus Spach Towner (1977)
4l. C. berlandieri Spach
42. C. hartwegii (Benth.) P. H. Re
43. C. lavandulifolius (Torr. & A. Gray) P. H. Raven
44. C. serrulatus (Nutt.) P. Н. Raven
45. С. toumeyi (Small) Towner
46. C. tubicula (A. Gray) P. Н. Raven
Clarkia Pursh Lewis & Lewis (1955, except in *)

47. C. amoena (Lehm.) A. Nelson & J. F. Macbr.

162 Annals of the
Missouri Botanical Garden

Table 1. Continued.

Taxa Source of information

48. C. biloba (Durand) A. Nelson & J. F. Macbr.

49. C. concinna (Fisch. & C. A. Mey.) Greene

24 C cylindrica (Jeps.) F. H. Lewis & M. R. Lewis

C. dudleyana (Abrams) J. F. Macbr.

ЕМ C. epilobioides (Nutt. ex Torr. & A. Gray) А. Nelson & Macbr.

53. C. gracilis (Piper) A. Nelson & J. F. M

54. *C. heterandra (Torr.) F. H. Lewis & P. H. Raven Lewis (1993)
55. C. lassenensis (Eastw.) F. H. Lewis & M. R. Lewis

56. C. modesta Jeps.

57. *C. mosquini E. Small Lewis (1993)
58. C. pulchella Pursh

59. C. purpurea (Curtis) A. Nelson & J. F. Macbr.
60. C. rhomboidea Douglas

61. *C. rostrata W. S. Davis Lewis (1993)
62. C. speciosa F. H. Lewis & M. R. Lewis
63. *C. tembloriensis Vasek Lewis (1993)

64. C. unguiculata Lindl.
65. C. xantiana A. Gray
Саига L. Raven & Gregory (1972)
66. С. i Michx.
67. G. biennis
68. С. boquillensis P. Н. Raven & D. P. Greg.
69. G. brachycarpa Sma
70. А calcicola : H. Raven & D. P. Greg.
11. occinea Pursh
72. " Pis (Spach) Torr. & A. Gray
13. G. filipes Spach
74. G. hexandra Ortega
75. G. longiflora Spach
76. G. i P. H. Raven & D. P. Greg.
77. G. mutabilis
8. G. neomexicana a Wooton
79. G. parviflora Douglas ex Lehm.

-—
=

80. " sinuata Nutt. ex Ser
81. suffulta gel ex A. Gray
82. А теи Torr.
Gayophytum A. Juss. Lewis & Szweykowski (1964)
5 G. decipiens F. H. Lewis & a is
C. diffusum Torr. & A. Gra
5 C. heterozygum F. H. Levis & Szweykowski
C. humile A. Juss
ғ. racemosum Torr. & A. Gray
88. G. ramosissimum Torr. & A. Gray

Gongylocarpus Cham. & Schltdl. (transferred to Gongylocarpeae; Levin et al., 2003)

89. G. rubricaulis Schltdl. & Cham. Carlquist & Raven (1966)
Oenothera L.

90. O. albicaulis Pursh W. L. Wagner e data)
91. O. biennis L. Dietrich et al. (1997)

92. O. brachycarpa A. Gray W. L. Wagner (unpublished data)
93. 0. caespitosa Nutt. Wagner et al. (1985

94. O. californica (S. Watson) S. Watson W. L. Wagner (unpublished data)
95. O. cavernae Munz Wagner et al. (1985)

96. O. cordata J. W. Loudon Dietrich & Wagner (1988)

97. О. coronopifolia Torr. & А. Gray W. L. Wagner (unpublished data)

98. O. deltoides Torr. & Frém. W. L. Wagner (unpublished data)

Volume 91, Number 1 Katinas

et al.
5 Diversification

163

Table 1. Continued.

Taxa

Source of information

99. 0. — Loes.) Munz

100. O. diss . Gray ex S. Watson

101. 0. ps Hook.

102. O. elata Kunth

103. : iil Kunth

104. 0. falfurr | Dietr. & W. L. Wagner
105. 0. flava (A. ч son) Garrett

106. O. fruticosa L.

107. O. grandiflora Нех

108. O. grandis (Britton) Smyth

109. O. heterophylla Spach

110. O. howardii (A. Nelson) W. L. Wagner
111. O. humifusa Nutt.

112. О. jamesii Torrey & A. Gray

113. 0. kunthiana Spach) Munz

114. O. laciniata Hill

115. О. latifolia | Rydb.) Munz

116. O. linifolia Ni
117. O. longissima Rydb.

—

118. O. macrocarpa Nutt.

119. O. macrosceles А. Gray

120. O. mexicana Spach

121. O. nuttallii Sweet

122. O. nutans С. F. Atk. & Bartlet

123. O. oakestana (A. Gray) J. M. ое ex S. Watson & J. M. Coulter

124. 0. pallida Lindl.

125. O. parviflora |

126. 0. pennellii Munz

127. O. perennis L..

128. O. pilosella Raf.

129. O. primiveris А. Gra

130. O. pubescens Willd. ex Spreng.
131. : purpusii Munz

132. € و‎ Nutt. ex Torr. & A. Gray
133. rosea l Hér. ex Aiton

134. 0. spachiana Torr & A. Gray

139. 0. villosa Thunb.
Stenosiphon Spach
140. S. linifolius (Nutt.) Hevnh.
TRIBE EPILOBIE Ak
Chamerion (Raf.) Raf.
141. C. angustifolium |.
142. C. latifolium L.
Epilobium L.

2. anagallidifolium Lam.

arcticum San

V
E
145. E. brachycarpum С. Presl
E. canum (Greene) P. H. Raven
47. E. ciliatum Raf.
148. E. clavatum Hausskn.

Wagner ERE unpublished data)
Wagner (1°
Dietrich "i m (1988)
Dietrich et al. (1997)

W. L. Wagner (unpublished data)
Ditri h & Wagner (1988)
Же r (unpublished data)
ira 1977)

Die sie A et al. (1997)

Dietrich & Wagner (1988)
Dietrich & Wagner (1988)

W. L. Wagner (unpublished data)
Dietrich & gue (1988

Dietrich et al. 97)

—

. L. Wagner nie d. data)

Dietrich & Wagner (1988)

" ЗЗА qiie d data)
Straley (1977)
ege h et al. (1997)
„ Wagner a d data)
liie i et al. (198
Dietrich & Wagner as
W. L. Wagner жй уз, xd data)
Dietric h et al. (1997)
Dietrich et al. (1997)
W. L. Wagner (unpublished data)
W. I. Wagner (unpublished data)
W. I. Wagner (unpublished data)
Straley (1977)
Straley (1977)
Wagner (1986, unpublished data)
Dietrich & Wagner (1988)
Wagner (2004, era data)
Dietrich & Wagner (1988
W. L. е e dala)
Straley (1977)
W. L. Wagner (unpublished data)

a Wagner (unpublished data)

|

W. I. Wagner (unpublished data)
|
|

г Ss

=

a Wagner (unpublished data)
a Wagner (unpublished data)

reat Plains Flora Assoc. (1986)

Hoch (1993)

Mosquin (1966)

Small (1968)

Hoch (1986, 1993. unpublished (
text))

See

164

Annals of the
Missouri Botanical Garden

Continued.

Table 1.

Taxa

Source of information

е
©
ج‎

]. coloratum Spreng.
,. davuricum Fisch. ex Hornem.
7. densiflorum (Lindl. H Hoch & Р. Н. Raven
d Ruiz av.
um (Nutt. ex Torr. & A. Gray) Suksd.
1 Barbey
halleanum Hausskn.
hornemannii Rchb.
. lactiflorum Hausskn.

— —
gg
— Ф
= ج‎

leptocarpum Hausskn.

—
S
>

5

leptophyllum Raf.

luteum Pursh

minutum Lindl. ex Lehm.
mirabile Trel

—
2
8

nevadense Munz

*

7. obcordatum A. Gray

2
ел
=

7 oregonense Hausskn.

;. pallidum (Eastw.) Hoch & P. H. Raven
s. palustre L.

„ pygmaeum (Speg.) Hoch & P. H. Raven
с. saximontanum Hausskn.

7, smithii Н. Lév

". strictum Muhl.

8
ty
х
=

-E
t ج‎

1 ل ل‎
— >
г eS

7. suffruticosum Nutt.

173. E. Watson) Hoch & P. H. Raven

torreyi (S.

Raven & Moore (1965)

Raven & Moore (1965)

Raven & Moore (1965)

Raven & Moore (1965

—

from recent or unpublished taxonomic revisions,
supplemented with specimen label data from the
herbaria at MO and US (Table 3). Distribution re-
cords for Epilobium derive from nearly 100,000
specimens from more than 100 herbaria consulted
in preparation for a revision (Hoch et al., unpub-
lished); these records served as the basis for Epi-
lobium treatments in The Jepson Manual (Hoch,
1993), the Flora of the Great Plains (Hoch, 1986),
and other recent floras. Records for several sections
of Oenothera for which taxonomic revisions are not
yet published (cited in Table 1 as “Wagner,

unpublished Oenothera distributions except for
those of section Anogra are based on approximately
4500 collections from more than 100 herbaria bor-
rowed for those revisions. For the 10 species of
section Anogra, distributions derive from some 250
collections at US and MO, supplemented by addi-
tional collections examined for The Jepson Manual
project (Wagner, 1993). We have excluded from our
distributional analysis specimens that were culti-
vated and/or appear far outside the established
range in human-disturbed habitats. Species that oc-
cur only in one area of endemism are not infor-
mative in
(PAE) regarding area relationships and therefore

Parsimony Analysis of Endemicity

are excluded from the analysis. However, they pro-
vide support for the delimitation of areas of ende-
mism and are listed in Table 2. For example, the
monotypic genus Xylonagra is endemic to Central

aja California and thus is used to circumscribe
the Sonoran (SON) region.

Although almost all of the genera of Epilobieae,
Gongylocarpeae, and Onagreae are endemic to or
have had their major basal radiation in the Mad-
rean Floristic Region of southwestern North Amer-

a, many species of these tribes, especially in Epi-
lobium and Oenothera, occur outside of North
America. If native North American species also
have a native distribution outside of North America,
those distributions are included in the data matrix
in the appropriate area (NE, WP, or EP). However,
if a species occurs as a native only outside of Nort
America, it has been excluded from this analysis.
These excluded taxa include in Epilobieae 6 Eur-
asian species of Chamerion and 125 species of Epi-
lobium (large groups endemic to South America,

cies each of Camissonia (C. dentata), Clarkia (C.
tenella), and Gayophytum (G. micranthum), and 39
species of Oenothera, virtually all endemic to South
America. In Epilobium and Oenothera, we have ex-
cluded 9 species (E. billardierianum and E. ko-

Volume 91, Number 1 Katinas et al. 165
2004 a Diversification

Table 2. Alphabetical list of areas of endemism used in this analysis, and taxa of tribes Epilobieae, Gongylocarpeae,
and Onagreae (Onagraceae) endemic to specific individual areas (see Table 1 for sources of distributional data). See
Appendix 1 for full descriptions of the areas and references: numbers in parentheses refer to Appendix 1

Acronym/Area of endemism Endemic taxa
APP/Appalachian (3) Gaura demareei Р. Н. Raven & D. Р. Greg.; Oenothera argillicola Mack.
ARC/Arctic (1)
ATL/Atlantic and Gulf Coastal (4) Gauri lindheimeri Engelm. & A. Gray; Oenothera clelandii W. Dietr., P.
. Raven & W. L. Wagner, O. yis Small
CAL/Californian (9) Camissonia benitensis P. Н. Raven, C. bistorta (Nutt. ex Tor
Gray) P. H. Raven, C. Aden a Р. Н. Raven, C. ed ы А P H.

Raven: C. luciae P. H. Raven, C. — (Hornem. ex Spreng.) P.
H. Raven: Clarkia a . H. Lewis & M. H. Lewis, C. borealis E.
Small. C. bottae (Spach) F. H. pues, & M. К. Lewis. C. breweri (A.
Gray) Greene, C. davyi 8 F. H. Lewis & M. R. Lewis, C. deli-
cata (Abrams) A. Nelson & J. F. Macbride, C. franciscana F.

Lewis & P. H. Raven, C. imbricata F. H. Lewis & M. Н. Lewis, С.
Joloensis D. R. Parn.. C. lew › Н. Raven & D. R. Pan “б

trata F. H. Lewis & M. К. + "wis, C. po (Lindl.) F. H. Lewis
NM „ similis F. H. Lewis & V. R. Ernst: Жайы ium
cleistogamum (Curran) P. Hoch & P H . Raven; Gayophytum oligo-
spermum F. H. Lewis & Szwey

CS
—
x
2
>
Ф
[

^
=
—
-
а
Л
~

CAN/Canadian (2) —
CHI/Chihuahuan (12) Gaura macroc a Rothr.: Oenothera eos S. Watson. O. neomexi-
'an all) Munz, O. organensis Munz, О. demie P. H. Raven
). " Tam. О. "isindii W. L. Wer, О. texensis P. Н. Raven &
D. R.
EP/East Palearctic (20) — (some e мей mies, but outside "4 North American 1 group)
GBA / Great Basin (8) . atwoodii Cronquist, C. confertiflora (P. H. Raven) P. Н. Ra-

C. exilis (Р. Н. Raven) P. Н. Raven, С. pere 4
Es (S. Watson) P. H. Raven. C. megalantha ud H.
Raven, C. neradensis (Kellogg) P. H. Raven, C. parryi (5. Watson) P.
H. Raven, C. speculicola (P. H. Raven) P. H. Raven

@
=
c
3

MAS/Mexican Altiplano (16)

MOJ/Mojavean (10) Ca munzii (P. Н. Raven) P. Н. Raven

NAP/North American Prairies (5) Gaura triangulata Buckl.; Oenothera canescens Torr. & Frém., O. coryi
W. L. Wagner, O. SERIE (Small) Munz, O. harringtonii W.
Wagner, Stockh. & W. M. Klein

NE/Neotropical (19) — (some endemics, but outside of North American study group)

ROC/Rocky Mountain (7) Mr 7, acutissima . L. Wagner, O. psammophila ( (A. Nelson & J. E

acbr.) W. L. Wagner, Stockh. & W. M. Klein
SMO/Sierra Madre Occidental (14) pilum ма a куйу. Oenothera maysillesti Munz. O. tamrae M.
т. & W.

SMR/ Sierra Madre Oriental (17

—

отойт мл NT. O. stubbei W. Dietr., P. H. Raven & W. L.
Wag

SMS/Sierra Madre del Sur (18)
SON/Sonoran (11) Cao angelorum (S. Watson) P. H. Raven, C. crassifolia (Greene)
Р. Н. Raven, С. proavita Р. Н. Raven, С. scies ul (Brandegee)
P. H. Raven; Gongylocarpus po» (Benth.) K. Brandegee; Oen-
othera arizonica (Munz) W. L. Wagner, O. 1 (Munz) P. H.
Raven, O. breedlovei W. Dietr. & W. L. Wagner, O. wigginsii W. M.
Klein: e e arborea (Kellogg) J. D. Smith & J. N. Rose
TA M/Tamaulipan (13) —
TMV/Trans-Mexican Volcanic Belt (15)
VAN/Vancouverian (6 Camissonia sierrae P. H. Raven; Clarkia arc иша (Kellogg) A. Nelson &
acbr., С. месе E. Small, C. exilis F. H. Lewis & Vasek, C
lingulata F. H. Lewis & M. R. Lewis, C. mildrediae (Heller) F. H.
ewis & M. R. Lewis, C. springvillensis Vasek, C. stellata Mosquin,
C. virgata Greene, C. williamsonii (Durand & Th ) F. H. Lewis &
M. R. Lewis; Epilobium howellii P. Hoch, E. nivium T. S. Bri Vs a
E. oreganum Greene, E. rigidum Hausskn., E. yk ais (D. I
Keck) Bowman & P. Hoch, E. siskiyouense (Munz P. Hoch & P.
Raven: Gayophytum d ж a Coville; Oenothera w ойи (Munz) P
H. Raven, O. xylocarpa C ville
WP/West Palearctic (21) — (some endemics, but e ч of North American study group)

—

166

Annals of the
Missouri Botanical Garden

Figure 1.
ч data for ж th species. The
ESRI) with a North A

marovianum from Australasia and
montanum, E. obscurum, and E. parviflorum from
Eurasia, O. glazioviana, a hybrid of recent origin

E. hirsutum, E.

in Europe, and O. mollissima and O. stricta from
South America) because all of them clearly have
been introduced into North America in historical
time.

PARSIMONY ANALYSIS OF ENDEMICITY (PAE)

Parsimony analysis of endemicity or PAE (Ro-
sen, 1988; Rosen & Smit
biogeographical approach that seeks to identify the

is an historical

ere drawn in Photoshop 7.0 by A
American Ташын conformal conic projection. The floristic regions are based primarily on
ha (1986) a Thorne (1993), with other modifications as described in the tex

Areas of endemism as oe for the historical i pud кип analysis and used to code the distri-

lice Tangerini on a base map from Arc

distributional pattern of organisms. It classifies lo-
calities, quadrats, or areas (which are analogous to
taxa) by their shared taxa (which are analogous to
characters) according to the most parsimonious so-
lution resulting in a hierarchical classification of
the geographic units (Morrone & Crisci, 1995; Cris-
ci et al., 2000, 2003). Rosen (1988) originally pro-
posed the method using localities as study units.
Craw (1988) and Cracraft (1991) presented a vari-
ation of the method using areas of endemism as
study units to identify the hierarchical information
contained in the geographical distribution of organ-

Volume 91, Number 1
2004

Katina

et al. 167
о Diversification

isms to establish area relationships. Indeed, Me-
Laughlin (1992) suggested that areas are actually
arranged in a natural hierarchy.

The variation of the methodology proposed by
Craw (1988) and Cracraft (1991) using areas of en-
demism included taxonomic information in the ma-
trix by adding columns for higher taxonomic cate-

gories or phylogenetic information. Thus, the

resulting matrix consisted of areas X species dis-
tributions plus generic distributions. However, as
Crisci et al. (2000) observed, adding phylogenetic
or taxonomic information to the matrix is a misuse
of Brooks parsimony analysis (Brooks et al., 2001).
which is a technique that does not utilize phylo-
genetic data specifically. Therefore. we use areas of
endemism as our units of study and species distri-
butions as the characters of those areas. but ex-
clude the information on supraspecific taxa.

PAE cladograms represent nested sets of areas
in which terminal dichotomies represent two areas
between which the most recent biotic interchange
1995).

reversions in the

has occurred (Morrone & Crisci. Craw
(1988) suggested that "character"
cladogram could be interpreted biogeographically
as extinctions, and parallelisms as dispersions. This

alysis was carried out using PAUP*, vers. 4.0b10
(Swofford. 2001). applying the branch-and-bound
and deltran options. If more than one tree results
tree Is

from the analysis, a strict consensus con-

structed. As proposed by Rosen (1988). the clad-
ogram was rooted with a hypothetical area coded
with all zeros. The bootstrap method (Felsenstein,
1985) was employed to evaluate the reliability of
the estimates; 100 replicates were performed. We
used the software MacClade 4.0 (Maddison & Mad-
dison, 2000) to generate the data matrix and as a
tool to analyze the taxa distribution on the tree(s).

PANBIOGEOCRAPHY (a )MPATIBILITY TRACK
METHO

Croizat (1958) postulated that geographic barri-
ers evolve together with biotas. The panbiogeo-
graphic approach (Croizat, 1958, 1) consists of
plotting distributions of taxa on maps and connect-
ing their separate distributional areas together with
lines called individual tracks. When individual
tracks coincide, the resulting summary lines are
considered generalized tracks, which indicate the
pre-existence of ancestral biotas that became frag-
mented by tectonic and/or climatic changes. At the
same time, generalized tracks provide spatial cri-
teria for biogeographic homology (Grehan, 1988a,
b: Morrone & Crisci, 1995). When two or more gen-
eralized tracks intersect, that area is called a node.

Nodes are dynamic biogeographic boundaries
where remnant fragments of different ancestral bi-
otas come into contact. Nodes are biogeographically
interesting because they are composite regions that
represent an intersection of different biogeograph-
ical and ecological histories.

Analvtical developments by McAllister et al.
(1986). Page (1987), Connor (1988). Craw (1989),
and Henderson (1990, 1991) used graph theory to
provide objective and quantitative methods for
drawing and comparing tracks, including the com-
patibility track method applied here. This method
was developed by Craw (1988, 1989). based on the
concept of distributional compatibility (Connor,
1988: Craw, 1989).

biogeographic hypotheses of relationship among lo-

Individual tracks are treated as

calities or distribution areas. Two or more individ-
ual tracks are regarded as being compatible only if
they. result in the same pairwise comparison or if
one track is a subset of the other. This method is
analogous to character compatibility (Meacham,

1984).

nonoverlapping tracks are incompatible,

—

However, in the track compatibility method,
whereas
they would be compatible under the original taxo-
nomic concept. The compatibility track method ba-
sically consists of constructing a matrix (areas vs.
taxa), Where each taxon is scored as present (1) or
absent (О) in each area, and applying compatibility
analysis software to find the largest clique(s) of
compatible tracks. The method involves finding a
simple form of spanning tree linking localities or
distribution areas. The tree is constructed from the
largest clique of compatible distributions in a dis-
tributional compatibility matrix and is based on the
original concept of compatibility (nonoverlapping
tracks are also considered compatible). Therefore,
using a restricted concept of compatibility (only in-
dividual tracks that are either included within or
replicated by one another are compatible) the tree
(= clique) could contain more than one generalized
track. In this case, multiple generalized tracks
(groups) found in one clique will be formed only by
areas that are exclusive of each generalized track.
If more than one largest clique or several cliques
of considerable size are found, then a hypothesis of
existence of several generalized tracks linking the
localities or distribution areas in more than one way
can be considered (areas can be members of more
than one generalized track at the same time). Al-
ternatively, the intersection (i.e., those individual
tracks common to all the largest cliques) can also
be identified as a generalized track (Craw. 1990).
For more details and other applications of this

method see Craw (1988, 1989), Morrone and Crisci

Annals of the

168

Botanical Garden

issouri

M

0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 ая
0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 dM
0100100000 0000001000 0000100000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 AN
0000000000 OOOTOOOOTT 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 SWS
0000000000 OOOTOOTOOT 0000000000 0000000000 0000100010 0000000000 0000000000 0000000000 0000000000 HANS
0100000000 00010010II 0000000000 0000000000 0000000010 0000000000 0000000000 0000000000 0000000000 SVIN
0100000000 OTOTOOTOTT 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 AWL
0100000000 OTOTOOTOOT 0000000000 0000000000 0000010000 0000000000 0000000000 0000000000 0000000000 OWS
OTOOOOOOTT TTOOTTOOTT 1110000000 0000000000 OOOOTOTIIT 0000000000 0000000000 0000000000 0000000000 WVL
TOOOOOOOTT TITTOOTOTT 1010000000 0000000000 0000TIIIII 0000000000 0000000000 0000000000 0100000000 IHD
TOTOOOOTOO OTOTOOTOOT 0000000000 TTOOOO00TO 0000011100 0001011000 0001000100 TTTOTOOOTT TTTOTTOTTO NOS
1000000000 0100000001 0000000000 0000000000 0000000100 1000001010 TOTTOTOOOT 0000000001 OTTOTTOTOO ГОИ
OOOTTITTOO 0000000000 OOOOOTTIIT IIOIIIIIII 1111000000 OOOTOTTOOT OOLLIOOIII TITOTTOTTT TOOTTTOTTO TWO
TOLTTITTOO OTOOOOTOOT 0000000000 TOTOOTOTOO 0000000110 IIIOIOIIII TTTTOTTOOO 0000001001 OTOOOTTTOL Vdd
TOTTTOTTOO OTTOOOOOOT 0000000000 TOTOOOOTOO 000000TTTO TTTOTOOTTO 0100001000 0001001100 000000TTOT JOY
OOTTTTTTOO 0000000000 O0000TTTTI ТТТТТТТТОТ TTTTO00000 OTTOOOLTTT TOTOTOTOTT OTTTOTOTOT TOOTOOOTOT NVA
TOTTOOTOTT TTTOOTOOTT 1101000000 0010000000 OOOOTOTITT 0010100000 0000000000 0000000000 0000001001 dVN
0000000001 TTOOTTOTTO OTOTTOOOOO 0000000000 000000TOTT 0000000000 0000000000 0000000000 0000000000 ILV
000000000T TTOOTTOTTO 0101000000 0000000000 000000TOTT 0000000000 0000000000 0000000000 0000000000 ddV
0000000000 0000000001 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000001000 NVD
0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 OHV
0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 LAO
06 08 OL 09 OS 0? 0€ 0c OT

1910 ¿dno13m()

"| = aouasaid Чу = s»uasqy “| e[qe] ur рипоу asoy) 0} spuodsa1105 ләдшпи uoxe] "ү xipuaddy pue z o[qe] ш pasty se әле вшАцоләрР рәте

= LAO `Аиәгшәриә jo sisÁpeue &uourisred. pue sisÁ[eue җәел Ánpiqueduios əy} 10у (9e99PIBRU() JO exe] [enprarpur sa seame ¡eoryder3o93) хеш vje(]

€ әче],

169

Katinas et al.

Volume 91, Number 1

2004

tion

Iversitica

Geographical D

000 0001000000 0001100000 TOOTOOTTTIT 0000000000 0000000000 0000000000 0000000000 0000000000 dal
000 000T000000 000TT00000 TOOOOOTTTT 0000000000 0000000000 0000000000 0000000000 0000000000 dM
000 0000000000 0000000010 0101000000 0000000100 1000000000 000000TTOT LTO 0100000000 AN
000 0000000000 0000000010 0001000000 0000100101 1000000000 0000000100 0000000000 SWS
000 0000000000 0000000000 0001000000 OOTOTOOTOT [000000000 0000000100 0100000000 YAS
000 0000000000 0000000010 0001000000 OOTOTOOTOT 1000000000 0000000110 1100000000 SYN
000 0000000000 0000000010 0001000000 OOTOTOOTOT 1000000000 0000000100 0000000000 0000000000 AWL
000 0000000000 0000000000 0001000000 OOTOTOOTOO 1000000000 0000000100 0000010010 0000000000 OWS
000 0000000000 0000000000 0000000000 OOOTTLOTOO 1000100000 OTOOOOTTTO 0000000010 WVL
000 0100000000 0000000000 0001110007 TTOTOTOTIO TTOOTOTOOO OTTOOOTIIO 0000010010 TOOTOOOTTO IHO
000 0000000000 0000001101 0001110000 0001000100 1 001000 0000000100 00000100II 0010001110 NOS
000 0000000100 0000000000 OOOTTTOOOT 0000000000 [100000000 0001000000 1000010000 OOTTOTTITOO ГОЙ
TOO OOTTTTOOOT ОТОТТТТТОТ OOTTTTOTTL 0000000000 ( )00000 0000000000 0000010010 0010001000 WO
LALO OTTTTTTTOT OTOTTTTOOT OOTTTTOTLL 0100000000 LI100001000 0001010000 000010010 OOTTOTTTOO үч)
TTO ТТТТОТТОТТ ТТТТТТТТОТ ТОТТТТОТТТ 0100000000 TOOOOOTOOL 0001010000 0010010 0001000100 JOY
TOO ТТТТТТТОТТ LELFLPLLLOLE OOTTTTOTTI 0100000000 0000001000 0000000000 0010000000 NVA
000 0111000000 OTOTTTOOOO OTOTOTOOOT TTOTOTTOTO 00000TTOOT OOTOTTITTO 0001000101 dVN
001 0001000000 0100000000 0101000001 OLOOLIIIOO QOLTOIOLLIO TOTOTOTOTT 0000100001 “LLY
001 0001000000 0100000000 OTOTOTOOOT LIOIIIIOIO OOTTOTOTIT TOTOTOTOTO 0000100001 ddV
001 0101000000 OLOILOOO000 LLOLOTLEEL 0100000000 OOTTOTOTOO 0000000000 0000000001 NV:
000 0101000000 TTTTLOO000 I00100IIII 0000000000 0000000000 0000000000 0000000000 0000000000 DUV
000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 0000000000 430
ELE Ө} 091 OST Ob 081 UCL ОТТ 001
“panuguor) се ou],

170

Annals of the
Missouri Botanical Garden

(1990, 1995), Craw et al. (1999), and Crisci et al.
(2000, 2003).

In this analysis we use the same areas of ende-
mism and the same data matrix (Table 3) that we
used in the PAE analysis. The analysis of the data
matrix of 2] areas of endemism versus individual
tracks of 173 taxa (Table 3) was carried out with
SECANT 2.2 (Salisbury, 1999), SECANT identifies
all groups of cladistically compatible characters.
Individual tracks were treated here as binary char-
acters ordered with absence as the “ancestral” state
for each (= outgroup with all zeros), and presence
as state
RESULTS
PARSIMONY ANALYSIS OF ENDEMICITY

The analysis of the data matrix (Table 3) with
PAUP*4.0b10 generated four area cladograms (Fig.
2) with 377 steps, consistency index (CI) = 0.459,
0.619, which differed
in the TT among most Mexican areas
SMO, V SMS; in the relationship
of the Neotropical area (NE) either with the Mexi-

and retention index (RI) =

can areas (Fig. 2B-D) or with the eastern North
American areas APP, ATL, NAP, CHI, and TAM
(Fig. 2A); in the relationship of APP, ATL, NAP,
CHI, and TAM either with the Mexican areas (Fig.
2A-B) or with the western areas VAN, CAL, ВОС.
GBA, SON, and МОЈ (Fig. 2C-D); and in the re-
lationship of Tamaulipas (TAM) either with Chi-
huahua (CHI) (Fig. 2C-D), or with APP, ATL, NAP.
and CHI (Fig. 2A-B).

The strict consensus of the four trees (Fig. 3)
shows the following area relationships: (1) (Arctic.
Canadian) West Palearctic, East Palearctic) forms
the basalmost lineage, sister to the remaining areas;
(2) (((Appalachian, Atlantic) North American Prai-
ries) Chihuahuan, Tamaulipas); (3) ((((Vancouveri-
an, Californian) (Rocky Mountains, Great Basin)
Sonoran) Mojavean); (4) ((Mexican Altiplano, Sierra
Madre Oriental) Sierra Madre Occidental,
Mexican Volcanic Belt, Sierra Madre del Sur); and

—

Trans-

(5) the Neotropical as one single branch. The last
four branches (2-5) constitute a polytomy. Thus.
the strict consensus cladogram generated by
PAUP*4.0b10 shows four main groups (Fig. 4):
northern North America, eastern North America,
western North America, and the central Mexican
areas.

The percentage of 100 bootstrap replicates dem-

—

onstrates that strength of support for nodes varies
Many branches have less than 50%
particularly in eastern and

considerably.
support, but others,

western North America, have stronger support. The

flora (15)

most strongly supported branches in order are: 99%
ATL), 98% (VAN—CAL), 96% (VAN, CAL,
ROC, GBA), 7996 (ROC—GBA), 78% (APP, ATL
NAP. CHI, TAM), 62% (VAN, CAL „ GBA
SON,
(ARC, CAN, WP, EP). The weakness and strength

of bootstrap values may reflect the strong concen-

-+

tration of taxa in northern Mexico and southwestern
United States, and lower concentration in areas
more distant from that area.

PANBIOGEOGRAPHY (COMPATIBILITY TRACK
METHOD)

Applying the SECANT 2.2 program to the data
matrix (Table 3) resulted in 4 largest cliques, each
with 51 individual tracks. The intersection (those
49 individual tracks common to the 4 largest
cliques) is considered as the fifth large clique.
These 5 cliques contain a total of 11 generalized
tracks. The first clique contains 2 generalized
tracks, the second clique contains 2, the third
clique contains 3, the fourth clique contains 2, and
the intersection contains 2 generalized tracks.
Since many of these tracks in different cliques are
the same, the 11 generalized tracks can be reduced
to 3 generalized tracks: 2 strongly supported
(“East”/green and “West”/purple in Fig. 5), and 1
weakly supported (“South”/orange in Fig. 5). The
northern regions (ARC, CAN, EP, and WP) and two
areas in Mexico (SMO and TMV) are not part of
these supported generalized tracks, and are shown

> л

”) strong generalized track in-
cludes eastern North American areas (ATL, APP,
CHI, NAP, TAM), and is strongly supported by 17
individual tracks from taxa in 3 genera, namely,
Calylophus berlandieri (taxon 41); Gaura biennis
67), С. brachycarpa (69), G. filipes (73), С. longi-
‚ б. sinuata (80), and С. suffulta (81); Es
Oenothera cordata (96), O. falfurriae (104),
grandiflora (107), O. grandis (108), O. dosis
(109), O. linifolia (116), O. mexicana (120), O. nu-
tans (122), O. spachiana (134), and O. speciosa
(135).

The second (“West”) strong generalized track in-

—

cludes the western North American areas (CAL,
GBA, MOJ, ROC, SON, VAN), and is supported by
31 individual tracks from taxa in 4 genera, namely,
Camissonia boothii (taxon 3), С. campestris (7), С.
graciliflora (15), C. lacustris (22), C. ovata (26), and
С. pubens (26); all species of Clarkia (47-65) ex-
cept for C. epilobioides (52), C. pulchella (58), and
C. purpurea (59); Gayophytum decipiens (83) and G.
heterozygum (85); and Epilobium clavatum (148), E.

Volume 91, Number 1 Katinas et al. 171
2004 Geographical Diversification

SMO SMO
TMV TMV
MAS MAS
SMR SMR
SMS SMS
C NE D | МЕ

Figur Four most erat cladograms (A—D) resulting from the parsimony analysis of endemicity (PAE)
analysis ils er pes na PAUP* vers. 4.0b10. Trees are 377 steps, СІ = 0.459, and RI = 0.619. Area acronyms
correspond to those in Figure 1 a Table 2.

172

Annals of the
Missouri Botanical Garden

Strict

Table

60
99
61
78
98
96

62

Strict

—

МЕ

consensus cladogram of the four cladograms obtained in the parsimony analysis of endemicity
(PAE). Bootstrap support values are shown above the branches. Area acronyms correspond to those in Figure 1 and

Volume 91, Number 1
200

Katinas et al. 173

Geographical Diversification

Figure 4. Strict consensus cladogram of the four ELS obtained in the parsimony analysis of endemicity

superimposed onto the m

with the areas of endemism. The

(ARC, CAN, EP, WP), ien North America (APP, ATL, NAP CHI, TAM), western No

ree branches delineate four main groups of areas: nort rthern

rth America (VAN, CAL, ROC,

GBA, SON, MOJ), and southern North America (SMO, TMV, MAS, SMR, SMS). Areas correspond to those in 1

1 and Table 2

densiflorum (151), E. glaberrimum (154), E. minu-
tum (161), E. Cee (165), E. pallidum (166),
and E. torreyi (173

The third (* ie >) E track includes
SMR, SMS) and

the Neotropical area (NE). with nia from only

some of the Mexican areas (MAS

2 individual tracks. of Oenothera deserticola (taxon
99) and O. epilobiifolia (103).

ized track is considerably weaker than the previous

The South general-

two, since it is supported by many fewer individual

tracks. The Neotropical area is supported as part
of the East generalized track by Oenothera lacinia-
ta (taxon 114). Belt

(TMV) is supported as part of the South generalized

The Trans-Mexican Volcanic

track by Oenothera kunthiana (taxon 113). Several
Mexican areas (SMS, TMV, MAS) are supported as
part of the East generalized track by Gaura drum-
(taxon 72) and Oenothera jamesu (112). As
the Sierra Madre Occidental (SMO)
does not form part of any generalized track.

mondii
noted above,

174

Annals of the
Missouri Botanical Garden

е 5. Distributional 1 after applying nd bu used analysis: a strongly supported Eastern gener-

Fig
alized track including APP, ATL NAP, and TAM, s

peal to those in Figure 1 and Table

These data weakly support the Neotropical area
(NE) as a panbiogeographic node in the distribu-
tional history of Onagreae, Gongylocarpeae, and
Epilobieae, since there is some support for its in-
clusion in both the East and South generalized
tracks.

The program SECANT 2.2 also found 9 cliques
each with 50 individual tracks. The analysis of
these 9 cliques resulted in the same generalized
tracks that we found among the five largest cliques,
with the exception of one generalized track found

the two non-North American areas EP and WP, do not form part of any senecalised track. Area acronyms

in only one of the 9 cliques. This additional track
includes the areas CHI and TAM, supported by
Gaura boquillensis (taxon 68), Oenothera macros-
celes (119), and O. pennellii (126).

Most of the genera of Epilobieae and Onagreae
support at least one of the generalized tracks found
in this analysis, i.e., Calylophus, Gaura, and Oen-
othera belong to the East track, and Camissonia,
Clarkia, Gayophytum, and Epilobium to the West
track. Several other genera, including Chamerion
(Epilobieae; two species), Gongylocarpus (Gongy-

Volume 91, Number 1
2004

Katinas

et al. 175
Geographical Diversification

locarpeae; two species). and Stenosiphon (Ona-
greae; one species) do not form part of any gener-

alized track.

DISCUSSION

The historical biogeography of North America
has long been a focus of botanists attempting to find
general patterns of relationships within North
North America and other
continents. The present-day geographical distribu-

America and between

tion of Epilobieae, Gongylocarpeae, and Onagreae
and the biogeographic patterns generated by those
distributions may provide clues to understanding
the high diversity and. endemicity of these three
tribes in North America, as well as the history of
the areas involved.
DISTRIBUTIONAL PATTERNS

The application of Parsimony Analysis of En-
demicity (PAE) to the species distribution of Epi-
lobieae, Gongylocarpeae, and Onagreae delimits
four major regions: northern North America; east-
ern North America; western North America; and
central Mexico (Fig. 4). Three of them (eastern
North America, western North America, and central
Mexico) are also found in the compatibility track
analysis. Comparison of these with the higher re-
gional floristic categories in the schemes of Takh-
tajan (1986) and Thorne (1993) suggests the follow-
ing differences and similarities. (1) Our northern
North American region coincides with the Circum-
boreal region of Takhtajan and Thorne. (2) Our
eastern North American region corresponds to the
North American Atlantic region of Takhtajan and
Thorne, with the addition of the Tamaulipas (TAM
and Chihuahua (CHI) areas. Miranda and Sharp
(1950) proposed such an affinity from distributions
of many plant species, and they and Berry (1930)
suggested that this shared flora was derived from
the Eocene Wilcox flora of the Mississippi Embay-
ment. (3) The Rocky Mountain and Madrean re-
gions of Takhtajan and Thorne show different affin-

—
—

ities in our analysis. Their regions proposed close
affinities between ROC and VAN, and among CAL,
GBA, and the Sonoran Province, whereas our re-
sults link VAN with CAL and ROC with GBA. Ra-
ven and Axelrod (1978) considered the Vancouver-
ian (VAN) and Californian (CAL) areas to be closely
related since they share a flora comprising a mix-
ture of northern temperate elements and xeric,
southern elements, with a very high degree of en-
demism. Furthermore, Axelrod and Raven (1985)
also considered the Rocky Mountains (ROC) and
Great Basin (GBA) areas to be close because Cor-

dilleran taxa spread into the western Great Basin
largely after 14 m.y. ago as the climate became
summer rains decreased, and eastern exotic
taxa were eliminated. (4) Our central Mexican areas
coincide with the Mexican Highlands Province of
Takhtajan and Thorne. The lower level of resolution

among the central Mexican areas observed in the

drier,

consensus PAE cladogram is most likely due to the
relatively few species of Epilobieae, Gongylocar-
peae, and Onagreae distributed there.

The relationships of the Madrean and other
North American regions to the Neotropical (NE) are
particularly complex, which is reflected in the am-
biguous position of NE in the four shortest trees
(Fig. 2). Indeed, NE could be considered a panbi-
ogeographic node in our study. Three species (Gau-
ra angustifolia [taxon 66], Oenothera humifusa
[111], and O. laciniata [114]) otherwise restricted
to the East region reach NE only at the southern
tip of Florida, and another eastern species, Epilob-
ium coloratum (149), occurs on Hispaniola (in NE).
apparently by long-distance dispersal. These taxa
provide support for NE as sister to the East region
(Fig. 2A). A single species, Gayophytum humile
(86), found primarily in the western region (VAN-
CAL-ROC-GBA), also occurs in NE, apparently as
a result of long-distance dispersal to central Chile
and Argentina (Lewis & Szweykowski, 1964). Most
of the connections of North American regions with
NE, however, are through the Mexican region (Fig.
2B-D). almost always by close adjacent dispersal
in western and southern Mexico, extending south
to Central and sometimes South America. Recent
phylogenetic analysis of Onagraceae (Levin et al..
2003, 2004) suggests the following: (1) the imme-
diate sister clade to the Gongylocarpeae + Epilo-
bieae + Onagreae is a branch with Lopezia (Lo-
pezieae) and Megacorax (unplaced). both found

primarily or exclusively in the central Mexican re-
gion, with some Lopezia species extending to NE;
and (2) each of the three successive basal clades
of the family, namely Fuchsia + Circaea, Hauya.
and Ludwigia, have primary or exclusive distribu-
tions in NE. Circaea, with its circumboreal distri-
bution and absence from NE, is a notable excep-
tion; however, it forms a strongly supported clade
with Fuchsia. A detailed analysis of biogeographi-
cal patterns in Onagraceae using phylogenetic in-
formation 1s now in progress.

The distributions of numerous species do not co-
incide with the major patterns found in the PAE
and track compatibility analysis. In general. these
inconsistencies can result from one of three types
of processes, namely, dispersal, vicariance, or ex-

tinction affecting one or few species. The predom-

176

Annals of the
Missouri Botanical Garden

inant process in our study appears to be short-dis-
tance dispersal into geographically contiguous but
unrelated areas. This may involve large-scale dis-
persal, but more often involves only a few or even
one population(s) in the adjacent area. For exam-
ple, many species with distributions in the East
North American region often extend into the CAN
area [North region; e.g., Oenothera biennis (91), O.
fruticosa (106), О. parviflora (125)]. or into ROC

est region; e.g., Calylophus serrulatus (44), Oen-
othera nuttallii (121)], or to the south into the Mex-
ican region [e.g., Gaura drummondii (72), Oenoth-
era jamesii (112)]. Similarly, some western species
reach CAN [Camissonia breviflora (4)] or even ARC
[along the southwest coast of Alaska; Epilobium lep-
tocarpum (158), E. luteum (160)] in the northern
region, or CHI [Camissonia chamaenerioides (9),
Epilobium canum (146)] or NAP [Camissonia an-
dina (1), C. subacaulis (38), Gayophytum ramosis-
simum (88)] in the East region. One particularly
clear example of gi pm ent dispersal concerns Oen-
othera primiveris (129); in the West region of
primary distribution (G BA, SON, MOJ), most pop-

ulations are large-flowered and outcrossing (includ-

©

ing some that are self-incompatible), whereas the
populations in CHI (Fast region) are small-flowered
and autogamous (Wagner, unpublished data).

Some distributions that seem to represent adja-
cent dispersal may in fact have another explana-
tion. For example, Oenothera villosa (taxon 139) oc-
curs widely in both the western and eastern regions,
suggesting adjacent dispersal. However, genome
and cytological analysis (Dietrich et al., 1997) of
this permanent translocation heterozygote species
shows that populations in the western and eastern
regions, which currently are treated as subspecies,
derived independently from different populations of
Oenothera elata 2) rtheless, they inter-

rade so extensively in the transition area between
ROC and NAP that they are best treated as sub-
species of a single species.

Several taxa may represent examples of long-dis-
tance dispersal. For example, Epilobium saximon-
tanum (169), found primarily in the western region
(ROC, GBA, VAN) with near outliers in the eastern
region (NAP, CHI), also occurs in eastern CAN
(Newfoundland) and ARC (Ungava Bay, Quebec) in
the northern region. This highly disjunct pattern is
not found in other species and seems best ex-

lained as a case of long-distance dispersal. The
distribution of Calylophus 5 (43) is
unusual in several ways: it appears “bimodal,” with
concentrations of populations in NAP (eastern) and
GBA (western) and relatively few populations in in-
tervening areas. In addition, the apparently normal

distribution in NAP + CHI + TAM in the eastern
region masks a long-distance disjunction between
populations in northern CHI and southern TA

Certain as inconsistent distribution pat-
terns may represent vicariance events. One pattern
am in Clarkia pulc hella (58) and three Epilob-
(156), E. lactiflorum (157),
A E. saximontanum (169)| concerns the occur-
rence of outlier populations of western taxa (in ROC
and VAN) in the Black Hills of South Dakota in
NAP (East region). The Black Hills, home to nu-
merous disjunct montane and northern taxa (e.g.,
Asteraceae: Balsamorhiza sagittata; Pinaceae: Pi-
nus contorta, P. flexilis; Ranunculaceae: Aconitum
columbianum; Van Bruggen, 1976; Great Plains
Flora Association, 1986), have become isolated as
the climate warmed in postglacial times; the pattern
seems best explained as an example of vicariance.
Similarly, at least six taxa (Camissonia confusa [12],
three Clarkia—C. epilobioides [52], C. purpurea
[59], and C. rhomboidea [60], and two Epilobium—
E. foliosum [153] and E. glaberrimum |154]) show
strongly disjunct distributions from southern Cali-
fornia (CAL and/or VAN) to south-central Arizona
(SON), mirroring a “trans-Sonoran Desert” vicari-
ance event described by Axelrod (19

Finally, the absence of taxa from certain areas in
which they may otherwise be anticipated may rep-
resent cases of local extinction. These are, however,

difficult to prove, and in some cases clearly do not
represent extinctions. For example, some species [4
of Camissonia—C. brevipes (5), C. d (11).
C. pallida (27), and C. refracta (34) and 2 of Oen-
othera—0. californica (94) and O. noe» (98)]
otherwise widespread in the western region are
missing in ROC. Yet their absence in ROC cannot
be considered extinctions, since all of these are de-
sert taxa with southwestern distributions quite dis-
tant from the ROC boundaries. On the other hand,
many taxa with the CAL + VAN (17 taxa) or CAL
+ VAN + SON (3 taxa) distribution patterns may
have become extinct in the adjacent MOJ area,
which has become progressively more extreme in
Holocene time, and progressively inhospitable to
many species (Axelrod, 1979) e absence of
many taxa in the MOJ region may have forced MOJ
into the position as the sister group to the rest of
the western region, when it may in fact be a more
recently derived area (Van Devender & Spaulding,
979).

The establishment of western and eastern North
American major regions found by PAE and track

—

„ analysis agrees with many previous
nalyses (e. g., Li, 1952; Croizat, 1965; Graham,
1972: Iltis, 1983; Xiang et al., 1998, 2000; Wen,

Volume 91, Number 1
2004

Katina

et al. 177
ea Diversification

1999: Guo & Ricklefs,
2001; Sanmartin et al., :
defined the two broad biogeographic units based on

2000:

These analyses have

Donoghue et al.,

the distributions of many taxa, some of which were
evaluated in a phylogenetic context.
those analyses, however, there exists a relationship
of these areas with East Asia. Disjunct North Amer-
ican—Asian taxa have been considered as Tertiary
relies with former ope distributions during
the Paleogene. “Arcto-Tertiary geoflora”

(Wolfe. 1978: Larsen,

tions

1980) resulted from migra-
North

through Beringia or across the north Atlantic. The

between eastern Asia and America
distributional patterns of Epilobieae, Gongylocar-
peae, and Onagreae show a close relationship be-
tween eastern and western North America. with
both areas more related to the Neotropics than to
weak association between

the Palearctic. and

northern North America and Asia. Our results do
not reject other hypotheses of such continental con-

The

analysis—the tribes Epilobieae. Gongvlocarpeae.

nections. taxa of Onagraceae chosen for our

display a biogeographical history
but that
can coexist at the same time. Our analysis does not

and Onagreae
that may differ from those of other taxa,

disprove the migration of taxa (including Epilo-
bieae, Gongylocarpeae, and Onagreae) through the
Atlantic
through the Panama isthmus.

northern land
The East and West
tracks show that two ancestral biotas existed on

Bering and bridges. or

both sides of North America, with the species of
each track sharing a common distributional history.

CORRELATION OF BIOGEOGRAPHIC
AND PALEOCLIMATIC

PATTERN WITH
GEOLOGIC EVIDENCE

The geological and climatic processes in the past
provide at least partial explanations for the current
biogeographical patterns in North America of Epi-
lobieae, Gongylocarpeae, and Onagreae. Major his-
torical events in this area include orogenic pro-
Rocky

the Sierra Madre. and western Cordil-

cesses such as the uplifting of the
Mountains,
lera. and the most recent glaciations (summary in
Graham. 1999).

The uplifting of the Rocky Mountains together
with the uplifting of the Sierra Madre Occidental
in the early Tertiary remarkably changed the biota
of western North America, creating a barrier for
floristic exchanges between eastern and western
North

flora of western North America: significant extinc-

America. This had two main effects on the

tion of taxa because of the increasingly dry climate

=

and accelerated speciation and diversification. of

new taxa (Qian, 2001). Indeed, the area of the

In many of

southern Rocky Mountains and the Sierra Madre
Occidental was an important center for the evolu-
tion of the Madro-Tertiary geoflora (Axelrod, 1958).
The early diversification of Onagraceae tribe Ona-
greae was postulated to have taken place in the
Madrean vegetation of western North America (Ra-
1978). ;

gylocarpeae, also endemic to the Madrean region,

ven & Axelrod, Until recently, tribe Gon-
was considered to be the basal branch of Onagreae
1966).
may have originated in western North America as
1976;
1994), but evidence from fossil pollen

(Carlquist & Raven, Tribe Epilobieae also

part of the Madro-Tertiary geoflora (Raven.

»

Baum et a
is equivocal, and the distribution of Chamerion and
Hs position as sister to Epilobium (Baum et al.,
904) suggest a possible origin in western Eurasia
(Raven & Raven. 1976).

Epilobium to the western track, and the endemism

The strong association of
of the near-basal species E. rigidum (Baum et al.,
1994; 2004) in the VAN region, sup-

port an origin of the genus in western North Amer-

Levin et al.,

ica. The Madro-Tertiary geoflora had already ap-
peared on the drier borders of the North American
tropics by the Middle Eocene, and probably occu-
pied much of the southwestern United States and
adjacent Mexico by the close of the Oligocene. It
extended its range in all directions in response to
the expanding aridity in the succeeding Miocene
1958: Valliente-Banuet et al.,
1998). Major expansion of Onagraceae tribes On-

epoch (Axelrod,
agreae, Gongylocarpeae, and Epilobieae may have
occurred during the Miocene and Pliocene (Raven
& Axelrod, 1974: 1976:
1979).

From the late Oligocene (25 mva) through the

Raven & Raven, Raven,

Pliocene, new orogeny gave rise to the present
western Cordilleran System, including major defor-
mation and uplift of the Rocky Mountains, Sierra
Nevada, Sierra Madre Occidental, and Sierra Ma-
dre Oriental (Axelrod € Raven, 1985: Wing. 1987:
1993)

climates that precipitated the development of grass-

Graham, . This resulted in cooler and drier

—

ands in central North America (Sanmartín et al..

2001).

western and the

being thus a third event differentiating the
Wen

(1999) noted that the close biogeographic relation-

eastern. floras. However,
ship between western and eastern North America

suggests that the Cordilleran range was not an ef-
fective barrier to exchange between these two flo-
ristic regions.

North
America experienced late Pleistocene full-glacial
conditions (20,000—15,000 vr. b.p.). late-glacial cli-
.000—10.000. vr.

Holocene interglacial conditions of the last 10.000

In the Quaternary period, the flora of

malic amelioration (15 b.p.). and

178

Annals of the
Missouri Botanical Garden

years (Graham, 1999). The Quaternary can be char-

acterized more by changes in the distributions of

plant taxa than by the evolution of new genera and
species (Delcourt & Delcourt, 1993). During times
of glacial maxima, fragmented populations may
have undergone genetic differentiation within iso-
lated refugia. With the onset of interglacial condi-
tions, migration and expansion of distributional
ranges would reestablish genetic exchanges be-
tween populations within species and among close-
ly related species that were formerly isolated. Gri-

—

chuk (1984) proposed the term “migration flora” to

denote floras that moved into a given region after
the preceding flora was eliminated by glacial or
and Delcourt

periglacial conditions. Delcourt

(1993) suggested that the individual elements of

such migration floras could move hundred to thou-
sands of kilometers as they differentially responded
to changing climatic and competitive conditions.
Different groups and species of Onagraceae tribes
Epilobieae, Gongylocarpeae, and Onagreae appear
to have participated in such Quaternary migrations
into western and eastern North America, apparently
from areas in the southwestern part of the conti-
nent. We hope that this scenario may be tested us-
ing other groups of plants and animals, as well as
other analytical tools including phylogenetic meth-

oads.

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Valliente-Banuet, A., N. Flores Hernandez, M. Verdu &
P. Davila. 1998. The chaparral Jegetation in tree 0

under non- Mediterranean climate
Madrean-Tethyan hypotheses rec considered.
Bot. 85: 1398-1408.

Van Bruggen, T. 1976. The Vascular Plants of South Da-
kota. lowa State Univ. Press, Ame

Van Deventer, T. R. & W. G. Spaulding 1979. Develop-
ment of vegetation and climate in the southwestern
United States. Science 204: 701—710.

1984 [1985]. Reconsideration of Oenothera

subg. Gauropsis (Onagraceae). Ann. Missouri Bot. Gard.

71: 1114-1127.

New ET in Oenothera (Onagraceae). Ann.

75—480.

Amer. J.

~)

ou Pp. 776-804 in J. C. Hick-

Volume 91, Number 1
2004

Katinas et al. 181
Geographical Diversification

man (editor), The Jepson Manual: Higher Plants of =

fornia. Univ. California Press, есейе and Los .
geles.
. 2004. Resolving a nomenclatural and taxonomic

оне m in аа ап Oenothera sect. Hartmannia (tribe
Onagreae, Onagraceae). Novon 14: 124-1: E
—— ———, R. E. Stockhouse & M. M. Klein.
tematics and evolution of the Oenothera е com-
Monogr. Syst. Bot. Missouri Bot

.T he syss

plex (Onagraceae).

Gard. 12: 1-103.

1999. Evolution of eastern. Asian and eastern

North American im hrs in flowering

plants. Ann. c col. 30: 421—455.

p. т ae 17 a 1993. Mammal
Species of ыч = Smithsonian Institution Press.
(www. va si.edu/m

Wing. S. L. 1987 ue ne and Oligocene floras and veg-

etation of 15 Rocky Mountains. Ann. Missouri Bot.
74: 748-784

d
Wolfe. J. ^. 1978, А paleobotanical interpretation of Ter “pe
tiary Јува) in the Northern Hemisphere. Amer. Sc

66: 694—703.
Xiang, О. V., D. E. Soltis & P. S. oe 1998. The «
Asian and eastern and western М

raster m

orth America floris

disjunction: Congruent phylogenetic patterns in sever

diverse genera. Molec db diu Evol. 10: 178-190.
سا‎

=]

21
Ww

ford. 2000. Tie the | "m

American floristic disjunction: "Muse ici с "m k corrob-

orates paleontological estimates. Molec. Phylogenet.
162—472

Evol. 15:

APPENDIX I.

North American areas of endemism used in this analysis;
tion. References for plant
endemics generally follow se th (1986); these are sup-
ple mented in some r & Christensen (1993).
in Canada by Aiken et de 309: (www.mun.ca/biology/
delta/arcticf/)); in California Ж Hickman (1993). and in
i Rzedowski (1978) and demi al et al.
Names were checked against the on-line Flora of
America database (dhttps//hua huh, harvand edi/
FNA). Endemic animals are arranged in the following or-
der: fish, amphibians, reptiles, b irda, mammals,
brates; within groups. alphabe tical by family. References ^s
animal endemics are Ric ketts et al. (199

see text for sources and explana

areas

inverte-

Mammals of the Reeder, ye
(www. — si. е, *Avibase (I epage. 2003: (www.
)sC-e0c.org ase)): ‘Amphibian Speci ies of the World
(Frost. отр p search.amnh / | hibia/))
Walkers Mammals of the World е “1997: (www.

press.¡hu.edu/books/walkers-mammals-of-the-world/)):
^Fishbase (Froese & Pauly, ap^ ura fishbase.org)): ‘Rep-
tile database (Uetz et al., 2003: (www. reptile-di itabase.
org): ' entomology (C alifornia E wis of Se iences, 2003:

2
l. Arctic (ARC ): includes nx of eoastal Alaska, north-
ern coastal Canada, all of the
chipelago, and Greenland.

ice-free Canadian Ar-
The flora is depauperate
in a nearly tree-less region of tundra and polar desert.
with fewer than 1000 species of vascular plants. En-
„= at the p level is moderate ( Aiken et al..

Asteraceae: Taraxact

E 'aceae: Brava orld: wulffu.
Caryophyllaceae: Cerastium regelii, Silene sorensenis:
Castilleja arctica;

99), e.g.: um hyparcticum:

Parrya arctica:

Orobanchaceae: Polemoniaceae:

Phlox richardsonii. Endemic fauna include Mammals
[Cervidae] Rangifer tarandus peary 1 (Peary caribou);
5 e 1 Lepus arcticus (arctic hare)!*:
ex pribilofensis (Pribiloff 15 lud shrew)'^.
ied n (CAN): fo

[Soricidae]

N

orms a broad band across Canada
Maska, ‚ош ө of ARC 5 north of Rocky Moun-

APP) regions, including
ew „England, Michigan, and Min—

=
5

Picea, Pinus, and Populus. Some endemic
glanis include Asteraceae:

naceae: Cryptantha rel Brassicaceae: Erys-
Silene williamsii:
Orobanchaceae: Cas-
tilleja annua; 5 eae: Eriogonum flavum: Por-
tulacaceae: Cla Primu
lasia gormanii. Endemic fauna include Маки
[Soricidae] Sorex gaspensis (Gaspe shrew)”:

Aster vukonensis; Boragi-

imum aspermum:; Caryophyllaceae:
Fabaceae: Astragalus ecosmus:

ytonia. bostockit: laceae: Doug-
Insects:
| Lepidoptera] Coenonympha nepisiquit (maritime ring-
let butterfly)!

расона (APP): includes а small part of southern
Ontario and Quebec, Canada, and most of the eastern
Unite ы States, excluding the Atlantic and Gulf Coast-
al region (ATL) to the south. Extends from central
southern Canada. and Minnesota to central
zark Plateau and the

w

a ita Mts.

Texas. In Texas.
nah" and "Blacklar
Johnston (1970).

eastern. dec peus est

1d Prairies’ areas of (

in Acer, Aesculu:
and 1 “Ma endemic plant species, including

nus serotina. Байоо fauna
[Р le ere pe welten (Black Moun-
: [Emydi ic lae] Clemmys

гоіса Битен (о ави»

~

'cupies ‘he "m

—
—
—
©,
~
=
-
=
z

4 Gulf Cod il (ATL): «

and “Guy

nelude Onagraceae h
wigia MR SUR L. pilosa, L. ravenii, and L. suffru-
ticosa, and undred species including
Annonaceae: Asimina incana; lridaceae: Iris hexago-
na; Lauraceae: Persea palustris; Pinaceae: Pinus el-
101tii; Se Salix floridana; Simaroubac eae:
Leuneria jM = ina; Тахасеае:
. Endemic fauna include. Reptiles [Testu-
dinidae] Caer us MR nus i жей tortoise)’;
Birds: [Corvidae] Aphelocoma coerule
cens (Florida serub jay)"; [Pi

several h

alic aceae:

Torre-

coerules-
cidae] Picoides borealis

182

Annals of the
Missouri Botanical Garden

їл

O

(red-cockaded woodpecker)'*; Mammals: [Ursidae]
Ursus piles ав Чеш black bear)’.
North American Prairies (NAP): includes prairies and
plains bres en the eastern кошш: “ч of API
on the east, the coniferous forests of RO
and CAN on the north, and the arid semi-deserts of
CHI and TAM to the southwest. Corresponds for the
most part with the “Great Plains” (Great P lains Flora
ut in Texas also includes the “Ed-
wards Plateau,” “Rolling Plains,”
areas of Correll and Johnston (197
dominant in this region, with a ric de mix ud pere nnial
forbs, and forest trees in some areas near rivers. No
endemic families, few endemic genera, some en-
demic species, including the Done Ринас еае:
Азс ин Fao an 1 Agavaceae: Yucca rupicola;
Lesquerella angustifolia; Fabaceae: As-
gracilis, Psoralea cuspidata; Polygonaceae:
Vale папас eae: Maer riana texana.

C on the west

xas blind s: e
and T. robusta (Blanco blind salamande aryl
* | Tympanuchus cupido (greater
prairie chicken) : Mammals: {Canidae} Vidoes velox
(swift fox)!2.
Vancouverian (VAN): extends as a coastal strip from
Kodiak Island in Alaska to coastal British Columbia,
widening in Washington and Oregon to include the
Cascade, Olympic, and Coast Ranges, extending into
California through the Klamath and Northern Coast
ranges in the west and through the southern Cascades
into the Sierra Nevada to its terminus in “ш
куле In Califonia, VAN Vp daa » the
‘aR, and SN regions of The Jepson os
un Ds 1993). x: onifers dominate T climax veg-
etation, along with some broad-leaved species of Acer,
Alnus, Cornus, Fraxinus, Populus, and Quercus. There
are endemic genera and some 500 to 600 endemic
species, including Apiaceae: Lomatium bradshawii;
Asteraceae: Aster =н Erigeron cervinus,
necio clarkianus; Iridaceae: Iris bracteata; Sarraceni-
aceae: Daring clari Taxodiaceae: Sequoia
sempervirens, Sequoiadendron giganteum. Endemic
fauna inc nds Fishes: [Catostor nidae] Catostomus rim-

iculus (Jenny Creek sucker)'^; [Cyprinidae] Gila bi-
color bicolor (Tui chub)'^: Amphibians: [Dicampto-
dontidae] Dic ampiadon ensatus (Pacific giant

salamander)'^; Birds: [Strigidae] Strix occidentalis
caurina (northern spotted owl)'^; Insects: [Lepidop-
tera] Colias behrii (Sierra sulfur butterfly).

ocky Mountain (ROC): includes the Rocky Moun-
tains and associated inland ranges from northern Brit-
ish Columbia
Oregon,

southwestern Yukon to central

south-central le a

and
extreme northeastern
Utah, and north-central New Mexico, bounded on the
west by VAN and GBA шш on the east by CAN and
NAP. In the extreme south, ROC borders the deserts
of CHI. Also includes some associated outlier ranges,
espec "nd extending to the east and south of the main
cordiller 1. Vegetation is zoned vertically, with Pi
ae maine dominant i in п the

of Abies, Junipe

тиў

=
=
"
(Л
^
*

tilleja gaat nos eae: oe

—
—

^
—

Phlox colubrina. Endemic fauna in-
: [Cyprinidae] Gila cypha (humpback
chub)'^; [айол не] Oncorhynchus clarki lewisi
(westslope cutthroat trout)'*; Mammals: [Mustelidae]
Mustela negripes (black-footed ferret)'?^; [Sciuridae]
Cynomys leucurus (white-tailed 8 8 dog) *
Great vies (GBA): bounded on the the Cas-
cade-Sierra Nevada axis (VAN), on thes ‹ “ast by pm
э оп he south by the desert regions ). S

nd CHI. In California, the boun ep ‘espn y to
hee of the MP and SNE (including White and
Inyo e regions of The Jepson Manual (Hick-
man, 1993). Includes the Snake River Plains of
southern Idaho and most of the Colorado P lateau, and

Polemon івседе:

clude Fishes

Che 5 eae, . and at higher elevations by some
combination of sp Acer,

; e, mancus;
packardiae: Papaveraceae:
naceae: meto. e Popoloca Primula
maguirei. fauna include Fishes: [Cyprini-
dae] Ptychocheilus lucius (Colorado pikeminnow)'^;
Mammals [| Helter cw Microdipodops pallidus
(pale kangaroo mouse

н їп (CAL): occupies a large part of the state
California, including the Central Valley, the Coast
en from the San Francisco region south into
northwestern Baja California Norte, Mexico, and the
Transverse Ranges of southern California. Bounded
on the northwest, north, and east by VAN, and on the
southeast by MOJ and SON oak & Axelrod, 1978 ).
Corresponds to the GV, CW,
Jepson Manual (Hickman, vegetation
varies altitudinally, from treeless grassland in lower
areas to chapparal and mixed forests of Aesculus, Pla-
tanus, Populus, Quercus, Salix, "a conifers at higher r
levels. Numerous endemic she

inc "s 8 Aste

Endemic

rac ене:

cophis e ruddocki (San Joaquin whipsnake)'";
Mammals s: [Canidae] Urocyon littoralis (Is Tand gray
fox)'?: [Hete romyidae] Dipodor ›туз оү d (giant kan-
D. venustus (narro
rat)"; Perognathus inornatus (San a aquin pocket
mouse)'?; Insects [Ley ор га, d Euphydryas
editha quino (с Juino checkerspot butterfly)’.
15 aih (MOJ): small but te region borders
ind CAL on GBA on north, and SON on
iin war east. Includes Death Valley, adjacent desert
ranges, and large desert region of d astern Cali-
fornia, to base of Tra responding to
DMoj region of The Jepson Manual (Hic 'kman, 1993).
Extends to east through southern Nevada and north-
weslern Arizona to extreme southwestern Utah
MacMahon, 2000). Predominately shrubby desert
dominated by endemic Joshua-tree Yucca brevifolia
(Agavaceae), with saltbush (Atriplex) scrub character-
istic of alkaline basins. Other characteristic species

garoo ral) ced kangaroo

west,

nsverse ranges,

Katinas et al. 183

Volume 91, Number 1
2004 Geographical Diversification

include Agavaceae: Yucca schidigera; Asteraceae:
Imbrosia dumosa; Cactaceae: Echinocactus polyce-
phalus, Ferocactus achantoides: and Zygophyllaceae:
Larrea divaricata subsp. tridentata. Some endemic
plants include Agavaceae: Yucca brevifolia; Astera-
ceae: An iphipappus | fremontii; Caryophyllaceae: Sco-
pulophila rixfordii; Cactaceae: Opuntia chlorotica;
i Penstemon calcareus; Polygonaceae:

жи лее, (Mojave киы squirre sh sect

thoptera, Ste nope Imatidae | Ammopelnat he a "sls
icket

(Kelso Dunes jerusalem cric
Sonoran (SON):
the MOJ in southeastern California, south ich
Baja ( oe Mexico, east through most of south-
western Arizona. and southeast 1 Sonora. Me *

ranges from the — n. border «

ico. Ve ry characteristic plants the region include
columnar cacti such as pie gigantea (saguaro)
and Pachycereus pringlei (Cactaceae). trees such as
Yucca valida (Agavaceae), Cercidium floridum. and C.
microphyllum (Cercidiphyllaceae). and shrubs such as
Acacia greggii (Fabaceae), Krameria grayi (Krameri-
aceae). and Larrea divaricata subsp. tridentata (Ave-
ophyllaceae). Endemie plant taxa include Onagraceae
(tribe Lopezieae): Lopezia clavata, and species in var-
ious other families; including Agavaceae: Agave au-
rea; Cactaceae: Opuntia rosarica; Fabaceae: Acacia
brandegeana, goldmanii, Errazurizia benthami:
Fouquieriaceae: Fouquieria columnaris; Lamiaceae:
Hyptis laniflora; Sapindaceae: Aesculus parryi: Sapo-
taceae: Sideroxylon peninsulare. Endemic fauna in-
clude Birds: [Emberizidae] Aimophila carpalis (ru-
fous-winged sparrow)": [Hydrobatidae | Oceanodroma
N e storm petrol, possibly ex-
l : Insects: [Coleoptera, Carabidae] Calathus

ine
peropacus nate ind imd Liebherr, 1991b). Pelma-
tellus parallelus (ground beetle)": [Hymenoptera, An-
e адан | Agapanthinus (digger bees; Ayala et al..

ne (CHI: borders SON and SMO on west.
GBA and ROC on north, NAP and TAM on east. and
MAS on south. Extends from eastern. Arizona and
central New Mexico through trans-Pecos Texas and
south into Mexico, including most of Chihuahua and
Coahuila. eastern. Durango. = northern Zacatecas.
Cooler desert than the Sonoran Desert. dominated by
a и и 5 tridentata und spe-
s of Acc Agave, Dalea, oe ra, Flourensia.
Prague 2 Jatr nhai among othe
|a, are found only along

. Trees, mainly

бы,
Es

spe e ie 5 0 исса and “
larger гоа ds. E dr. nic 1
osia johnstoniorum, Flaveria anomala.

mb
Gaillardia gypsophila: Chenopodiaceae: Meiomeria
Jalea fi

spec ie 8 Inc m ide As-

Fishes: [€ yprinidae| Campo ostoma ornatum (Mexican
stone eralle т). Notropis chihuahua (Chihuahua shin-
er): Reptiles: [Te ‘idae :] ente dh vin tigris vari-
oe ©; Insects [Coleoptera, d | Agonum ex-
timum (ground beetle; Liebherr, 1991a).
пена (TAM): ranges bon southeastern Texas
to western Coahuila and most of Nuevo León and Ta-
шош in Mexico. excluding southern parts of these
states. Bounded on west by CHI and SMR and оп

north in southern Texas by complex interface with
АР, APP, n Texas, corresponds to “South

grasslands, moister с Бе CHI desert to the west. Veg-
etation is largely open shrub- and grasslands with
Acacia, Aloysia, Celtis. — Кенен Ziz ziphus.
and other spiny species. Endemie plant species in-
clude Boraginaceae: He обара torreyi; Ebenaceae:
Diospyros palmeri: Euphorbiaceae: Croton torreyanus:
“abaceae: Acacia rigidula, Mimosa malacophylla:
auraceae: Phoebe tampicensis; Lentibulariaceae:
Pinguicula gracilis; Plantaginaceae: Lei set иц

oL
frutescens: нур eae: Polygala аши Rha

naceae: Condalia hookeri; Rutaceae: Amyris passi
Endemic fauna include Fishes: 5 —
тас Lin eae (Rio Grande cichlid): Mammals:
po iuridae] Cynomys mexicanus (Mexican prairie dog:
Fa & Morales, 1993)? : [Talpidae] Se riage montanis
(Coahuila mole): Inés ets: [Coleoptera. Carabidae
Platynus bacatellus (ground beetle: Lie nae srr, 1992),
Sierra Madre Occidental (SMO): borders SON and a
coastal strip of the Central American Neotropical area
(NE) on ipe and CHI, the Altiplano of central Mex-
nd the Trans-Mexico Volcanic (PMY) re-
gions on 1 east and south. Starts near U.5.-Mexico
border and extends southeast through western Chi-

huahua. Durango. a small part of Lac alecas, eastern
‘| ae main Cor-
terrain from
200 to 2200 m. with a pronounc i eastern ult. The
region is characterized by a variety of habitats. in-
cluding both dry and subtropic al on sls al lower el-
Lions. dry mixed forests at mid-elevations, and
pine ‘cloak forests above 2000 m. Endemic plants in-
clude Onagraceae (tribe Lopezieae): Lopezia ciliatula.
L. conjugens. L. ed L. laciniata, L. lopezioides. L.
ovata, L. semeiandra, L. sinaloensis. and L. suffrutes-

A
me]

cens, and species in various

\steraceae: Alvordia congesta, Hofmeisteria sinaloen-

sis. Perityle grandifolia} Cactaceae: Ferocactus

se "те arzii. Mamillaria rubidea, Stenocereus martinezii:
1 ria kimnachi

demic fauna ine dalle Pinda: Ms idae] Сатре күзү im-
pertalts (imperial woodpecker)': Insects: [Coleoptera.
Carabidae] Elliptoleus olisopoides (ground. beetle:
Liebherr, 1991 a); [Ne Is ra. Myrmeleontidae | Mar-
ac ا‎ apicalis (antlion

is- Mexican Volcanic FT TMV): extends in nar-
row. light northwest to sb eh band in central
Mexico. from central Jalisco and Guerrero oie a
southern Estado Mexico barely to Puebla. Borders
SMO and the coastal NE strip on west and south,
MAS on north, and a اا ا‎ O monlane area be-
tween SMR and SMS on east. Major
(3900-4000 m) covered by
coarse bunchgrasses Festuca tolucensis, Calamagros-
tis tolucensis, and кеу. уа e а мє

~
=
~

characteristic taxa included s s of / Al-

chemilla, Arenaria, Cerastium, P eaa 5
lus, and Trifolium. Among the very large number of
endemic plant species are Onagraceae (tribe Lope-
zieae): Lopezia d at least seven endemic al-
pine species of Asteraceae: Cirsium nivale, нізе зд
ium sarmentosum, 6. D E Senecio calcarius

184

Annals of the
Missouri Botanical Garden

o

—

N

S. gerberaefolius, S. procumbens, and S. roseus; and
many other taxa, inc luding Garryacea ae: Ga varrya lon-

era, O. cuernavacana. e Am-

: abria] Ambystoma (Rhyacosire-

rivularis oe ›асап strean ander)’;

ridae] Neotomodon altstoni Mex xican

volcano РЯ Reithr ys chryso,
ез OF

salan

ueipes (ground
91b), Platynus machetellus
(ground beetle; Liebherr, 1992); [Hymenoptera, An-
ا‎ Loxoptilus (digger bees; Ayala et al.,
1993).

и 1 (MAS): in central Mexico lies be-
CHI on north, the mountains of SMO on the
H an SMR on the east, and TMV on the south.
vas pear and io Zacatecas, southeast-
ern Durango, eastern Jalisc o and Michoacán, northern
Estado México, western San Luis Potosí and Hidalgo,
the Federal District, Aguascalientes, Guanajuato, and
Querétaro. This region is characterized by mixed, less
xeromorphic tree communities of Acacia, Ipomoea,
and Opuntia. Endemic dg spec ies include
Yucca queretaroen ; Aster aceae: Acourtia eli-
zabethiae; Berbe erberis albi ;acta-
ceae: Lophophora difin Mammillaria сазри һа;
Fabaceae: Асе oria; Lentibulariaceae: Pingui
ula ud Endemic fauna duds Insects: [Cole-
optera, oe е ici i beetles;
Liebherr. ticae] Para-

ea
тг

gava-
сеае:
eae:

1LC-

alictic >
Sierra Madre d (SMR): borders CHI anc Үй MAS
AM on east, including parts of southern
eon, cas, San
Luis Potosí and Hidalgo: most of Tlaxcala, western
са Veracruz and
tern Tamaulipas. A gically ongles
montane area with high levels of dun in the
slatively moist eastern part; lower elevations in the
5 support tropic әз ned forest. At middle
to higher elevations (10( 00 m), strips of warm-
temperate to subtropical о forest occur, with

erg

—
*

eastern Zacate

deciduous/semi-ev Pine m oak
t highest elevations. The mixed forest
contains genera c _ ‘teristic of the ae 'hian re-
gion, such as Carpinus, Cornus, “ч Hamamelis,
Liquidambar, Pinus, Platanus, and el

reen spec ies.

forest occur at

J

pse araceae: Clethra

agl oa; Fagaceae: Fa-
gus mexicana, Quercus germana, 0 rysophylla; Jug-
landaceae: Juglans mollis; Oleaceae: Forestiera race-
mosa; Meliosma alba. Endemic fauna
include Reptiles: [Anguidae] Abronia graminea (ter-
restrial arboreal alligator lizard)’ tae

Sabiaceae:

Liebherr, 1992); [Lepidoptera, Papilionidae; Llorente-
Bousquets & Luis-Martínez, 1993] Parides alexiares

P

—

~
—

(Oaxacan swallowtail), Priamides erostratinus (swal-
lowtail), Pre 7 0 1 5 si us (swallowtail).
Sierra Madre del 5 ir (SM w

eastern Guerrero, northwestern Oaxaca, and southern
Puebla and Morelos. Connects to r ith ' А
MAS, and SMR, but mostly surrounded by lowland

E th is o рап of t е 3

o
=”

Quercus and Janek as
of more 1 tropical derivation. En kis plants
include Onagraceae: (tribe Fuchsieae) Fuchsia ravenii
and (tribe Lopezieae): Lopezia smithii, as well as Aga-
vaceae: Yucca mixtecana; ipn 'eae: 5
mee Malvaceae: Hibiscus tenorii; s
tomataceae: Miconia ооа сасеае:
Muionthenum amoenum, M. mac dum M. com-
indemic fauna include Amphibians:
¡Ple nia Thorius grandis ied minute sala-
mander), T. infernalis (Atoyac minute salamander);
Reptiles: [Anguidae] Abronia deppii (alligator lizard);
Insects: [Coleoptera, d Calathus ovipennis,
Elliptoleus E E. whiteheadi (grounc

alors n bon platynellus (ground

22).

species

PE
LI

cense.

›ее-
tles; Liebhe

beetle; [ekhi
Neotropical (NE): k rge region, essentially the Neo-
tropical Kingdom E Takhiajan (1986), comprises ¢ ev-
erything south of t ac ш and North American
regions. For лийын of this analysis, NE includes а
road spectrum of tropical sub-regions, from the

Шш h the islands of the Caribbean ا‎ most of
the ا‎ plains of Mexico, and all of al
ica lo most of South а. Саа n very large
number of endemic plant taxa are e tribe
and nume Fuchsia (tribe
) and Ludwigia (tribe 1 airn and the
plant 5 пунан о ‘eae, Cyclanthaceae, Desfon-
lainiaceae, ircgraviaceae. Endemic fauna in-
clude 5 [Hylidae] Gastrotheca (Notodel-
phis) ovifera (giant marsupial frog)"; Reptiles: [Boidae]
subfamily Boinae (boas and Wer Birds:
i i mals”: [Camelidae] Lama
nas): family Caviidae (cav
family Chinchillidae (chinchillas and
; [marsupials, Microbiotheriidae] Dromi-
clops (monio 95 monte).
East Palearc EP):
Meise. е жө of the Cire жон а апа
ntially all of the diverse Eastern Asiatic Region
of "Takhtajan (1986), including the eastern ES as,
most of China, the Korean Peninsula, Japan and the
north Pacific Ocean island s ' a of this
in-

Amer-

—
—
—
o
=
=
a
e

rous spec ies

—

fam-

ies,

defined here to include the

The flor
ry rich in ӨШ н

е ral species of Circaea
(tribe Circaeeae; : Boao 1982) and Epilobium (tribe
Epilobieae; Chen et al., 1992), as well as the endemic
families C 8 e eae, Ginkgoaceae, and Trochod-
endraceae, and more than 300 endemic genera [e.g..
Apiaceae: Tetrapanax; Berberidaceae: Папанин 1; Cor-
naceae: Aucu
Chaenomeles; гур-
tomeria|. Endemic fauna include Fishes: [Siluridae|
Silurus asotus (Amur catfish)'; Reptiles-Crocodilians:
family Gavialidae (gharial)'; Birds [Phasianidae] Gal-

series,

Volume 91, Number 1 Katinas et al. 185
004 Geographical Diversification

lus gallus (red jungle fowl, chicken)’; Mammals?* or- plants, including Apiaceae: Agasyllis, Endressta, Tho-
der Dermoptera (flying lemurs); family Hylobatidae rella; As Berardia: Boraginaceae: Megacar-
(gibbons and lesser apes); [Leporidae] Pentalagus ]
(бшкп rabbit). sic
West Palearctic (WP): defined here to include Euro- Haberlea). Endemic an include F baba 8. Ге |
west Asian parts of the Cireumboreal Re Silurus aristotelis (Aristotle's саһ) Amphibians:
verything west of [Pelobatidae] Pelobates (European loa toads)!

Mammals: [Bovidae] Ovis musimon (mouflon sheep)

NS
—

pean and
gion (Takhtajan, 1986), essentially
EP in Eurasia. The flora includes many endemic

FLORAL BIOLOGY OF Peter Goldblatt,” Ingrid Nénni,* Peter
HESPERANTHA (IRIDACEAE: Bernhardt,* and John C. Manning?
CROCOIDEAE): HOW MINOR

SHIFTS IN FLORAL

PRESENTATION CHANGE

THE POLLINATION SYSTEM!

ABSTRACT

Field observations, floral dissections of a representative range of Hesperantha species, and pollen load analyses of
| Ji | |
ss pollina

insects ие оп тапу of them indicate that flowers of this African genus are
‘he i i

or nodding, salver-shaped, strongly fragrant, white flowers that open in the mid to late afternoon and evening and are

pollinated by long-tongued apid bees and/or noc ‘tuid moths. Species of the H. pauciflora type have a virtually identical

pink to mauve or m and the flowers are usually unscented and are
30

floral morphology. but “the perianth is yellow or
type are also pollinated

day, closing between midday and late afternoon, 16:30 H. Flowers of this ty
African winter-rainfall zone thes effective pollinators inc lude nemestrinid flies
osa a) with relatively short probosces and hopliine scarab beetles. In H. latifolia type flowers the perianth is pink
lo magenta or red (rare ly pale yellow), odorless, opens during the day but has an elongate perianth tube exceeding 18
mm in length. These flowers are pollinated mainly by arias sid flies in the genera Prosoeca and Stenobasipteron
(Nemestrinidae) or Philoliche (Tabanidae), but the "d flowers of H. coccinea are pollinated by a guild of large butterflies
including Papilio and the satyrid Aeropetes. Lastly, Н. vaginata has odorless and nectarless, short-tubed yellow flowers,
usually with contrasting dark markings, that open a during the day and are pollinated exclusively by the hopliine
scarab beetle, Clania gle nlyonensis. The taxonomic distribution of plant species with these pollination systems makes
it clear that shifts in pollination systems have occurred repeatedly across i oe although floral morphology and
nectar biochemistry are relatively conservative. Whether flowers are nocturnal, crepuscular, or diurnal, only four vari-
ables affect the floral ecology: length of the perianth tube, presence or absence of floral fragrance, m of anthesis,
species with pink, magenta, red, or vellow flowers close at night
ys fragrant and either open late

open during the
by apid bees, but in the scutbuin

and the closely associated trait of perianth color. Thus, s
and are rarely fragrant, whereas those with white or pale vellow flowers are nearly alwa
in the day or Gals at sunset and remain open for most of the night. Species show vinea rable variation in nectar
volume and sugar concentration, closely correlated. with pollination system, while two long-tubed species with floral
characters typical of long-proboscid fly pollination produce no nectar and are inferred to ы Batesian or guild mimics
that achieve pollination by deception

ey words: bees, flor al ecology, ao rantha, hopliine beetles, Iridaceae, long-proboscid flies, nectar, pollination
systems, settling moths.

The radiation and diversification of the African For example, Lapeirousia is pollinated by long-pro-
boscid flies, or bees and butterflies, or moths (Gold-
blatt et al., 1995). Romulea exploits scarab beetles,
pollen-collecting bees or, in at least two species,

go

Iridaceae depend to a greater or lesser extent on
the plasticity of pollination mechanisms, and all the
larger genera of the family exhibit a wide range of
floral adaptations and correlated sets of insect or long-proboscid nemestrinid flies (Goldblatt et al.,
avian pollinators (Bernhardt & Goldblatt, 2000). 1998a; Manning & Goldblatt, 1996, and unpub-

! Support for this study by grants 5408-95, 9554-97, and 6704-00 from the National Geographic Society is gratefully
acknowledged. We thank Robert Brooks, Holger Dombrow, Douglas Kroon, H. Kruger, and Kim E. Steiner for their
help with the identification of insects; Margo Branch and John Manning for the illustrations; John Donaldson and his
group for sharing field. facilities at Nie uwoudtville; Neil MacGregor for allowing us to conduct our research on his
prope rty; and Cameron McMaster and Lendon Porter for assistance with fieldwork. Collecting permits were EUM

y the Nature Conservation authorities of Mpumalanga, Western Cape and Northern Cape dpi ‘es, South Africa.

B. A. Krukoff Curator of African Botany. Missouri Botanical Garden, Р.О. Box 299, St. Louis, Missouri 63166-
0299, U.S.A. peter.goldblatt@mobot.org.

s National Botanical Institute, P. Bag. X7. C laremont ШЕ South ES ‘a. ios nbi.a

St. Lo канш 63103, U.S.A. ber al du.

' Department of Biology, St. Саца Univers
Compton harkai National Botanical [ыш ‚ Вар. X7, шо е South Africa. manning@nbict.

=

nbi.ac.za.

ANN. MISSOURI Bor. GARD. 91: 186-206. 2004.

Volume 91, Number 1
2004

Goldblatt et al. 187

Floral Biology of Hesperantha

lished). The majority of species of Gladiolus appear
to be pollinated primarily by nectar-feeding apid
1998b).
but some red-flowered species are pollinated by the
arge butterfly Aeropetes (Johnson & Bond. 1994),

and anthophorine bees (Goldblatt et al..

while others are dependent on andrenid bees. a
combination of bees and hopliine beetles (Goldblatt
et al.. 1998a). long-proboscid flies, moths, or birds
(Goldblatt & Manning. 1998: Goldblatt et al., 1999,
2001).

Hesperantha, a mid-sized genus of subfamily
Crocoideae (syn. Ixioideae). comprises approxi-
mately 80 species (Goldblatt, 1984. 1986. 1987.
1993, 2003: Hilliard & Burtt, 1986; Goldblatt &
Manning. 1990) distributed from the southern tip
of Africa through the eastern African mountains as
far north as Ethiopia and Cameroon. Diversity is
greatest in southern Africa, where there are two
centers of diversity and regional endemism: the
Drakensberg of South Africa and Lesotho; and the
west coast and near interior of Northern Cape and
Western Cape Provinces of South Africa. Compared
with the approximately 260 species of Gladiolus.
the 50 species each of Ixia or Watsonia, or the 40
species of Lapeirousia, Hesperantha species have a
conservative floral morphology. The relatively small
flowers (tepals typically 10—25 mm long. exception-
ally to 37 mm) are radially symmetric, have sube-
qual tepals, and are arranged in slender to compact
spicate inflorescences. The flowers of most species
have a symmetrical androecium and a style that
diverges at the mouth of the floral tube into three
long. spreading branches. Interspecific floral vari-
ation is restricted to perianth tube length and de-
gree of curvature, perianth color (uniformly white
to cream vs. various shades of pink to purple, or
yellow, sometimes with dark markings). the pres-
ence or absence of fragrance, the type of floral odor,
and the timing of anthesis (Goldblatt, 1984. 2003).

A particularly unusual aspect of floral variation
within this genus is the close linking of floral pig-
mentation with the presence of floral odor and tim-
ing of anthesis. White- or cream-flowered species
of the southern African winter-rainfall zone are cre-
puscular or nocturnal and produce a strong floral
fragrance, whereas species with flowers of other
colors. and the white-flowered species of eastern
southern Africa, are typically odorless, at least to
the human nose. Field studies of the pollination
systems of a selection of Hesperantha species were
undertaken to define and compare intrageneric
trends in the evolution of pollination mechanisms

and the function(s) of floral traits.

MATERIALS AND METHODS

INFLORESCENCE PHENOLOGY AND FLORAL LIFE
SPAN

Direct observations are presented on 34 Hesper-
antha species made in the field from 1993 to 2002
(Table 1) and supplemented by living collections at
Kirstenbosch Botanic Gardens. Cape Town. and the
Missouri Botanical Garden, St. Louis. Observations
were made in the southern spring. summer, or au-
tumn at sites in southern Africa (August to April).
Observations of insect foraging involved 4 to 10
hours per plant species (or occasionally more) and
included recording of floral attractants (pigmenta-
tion, scent), rewards (nectar). the mode and timing
of anthesis (opening of individual buds), daily phe-
nology. anther dehiscence patterns. expansion of
stigmatic lobes, the behavior of insects on the flow-
er. and the taxonomic diversity of floral foragers.
Floral scent was noted in the field and in cultivated
plants. Scents too weak to be immediately dis-
cerned by the human nose were recorded after in-
dividual flowers were picked and placed in clean.
lidded glass jars and stored in a warm place. The
contents of each jar was smelled after a minimum
of 60 minutes (Buchmann, 1983). Plant voucher
specimens are deposited in the herbaria at the Mis-
souri Botanical Garden (MO) and Kirstenbosch Bo-
tanie Gardens (NBG) (Table 1).

COMPATIBILITY

Compatibility relationships were examined in
two species, Hesperantha quadrangula and H. pal-

lescens, both maintained in the laboratory and iso-
lated from possible pollinators. Fruit and seed set
were compared in five hand-selfed flowers and five
flowers crossed with pollen of another individual of
the same species. In the Iridaceae hand-selfing of
as few as five flowers is usually sufficient, as results
are seldom mixed. Either all self crosses result in
seed set or none do. Likewise. xenogamous crosses
always succeed.

NECTAR ANALYSIS

Nectar volume measurements were taken pri-
marily from unbagged flowers in the field, soon after
they opened, reflecting both rates of secretion and
depletion. To collect nectar, mature flowers were
picked and nectar was withdrawn from the base of
the perianth tube with 3 ul capillary tubes after
separating the ovary from the perianth base. The
percentage of sucrose equivalents in fresh nectar
was measured in the field or laboratory using a Bel-
lingham and Stanley hand-held refractometer (O—

188

Annals

of the
Missouri Botanical Garden

Table 1.

Manning) or at NBG (other collectors). All study sites are in South Africa.

Study sites and voucher information for Hesperantha species studied. Vouchers are housed at MO (Goldblatt

Species

Study site

Voucher

—

1.

‚ falcata (1..

. pilosa (L.

. radiata (Jacq.)
ite |

Н. scopulosa Hilliard
. similis (N. E. Br.

. spicata (Bu

. acuta (Lichst. ex Roem. & Schult.) Ker

А pu — Baker

. baurii Baker

. brevicaulis (Baker) G. J. Lewis
coccinea (Backh. & Has ) Goldblatt & J.

E

cuc m Klatt
erecta (Baker) Benth. ex Baker
f.) Ker Gawl.
ste

ite 2
flr Baker
flava G. J. Lewis
Possis Klatt
grandiflora G.
huttonii ш Hilliard & Burtt
lactea Baker
latifolia (Klatt) M. P. de Vos
leucantha Baker

. luticola Goldblatt

. marlothii R. C. Foste

. oligantha (Diels) Goldblatt

. pallescens Goldblatt

. pauciflora G. J. Lewis (pink flowers)

site 1

site 2

. pauciflora (yellow flowers)

f.) Ker Gawl. (blue flowers)

. pilosa (white flowers)

site
site 2

site 3

. pseudopilosa Goldblatt
‚ pubinervia Hilliard
. quadrangula Goldblatt

Ker Gawl.
Site

Site 2
. rivulicola Goldblatt

.) R. €. Foster
urm. f.) Ker Gawl.
stenosiphon Goldblatt

. sufflava Goldblatt
. vaginata (Sweet) Goldblatt

woodii Baker

Western Cape, foot of Vanrhvn's Pass
| \

Glenlyon, Nieuwoudtville
Free State,
Mpumalanga, God’s Window

The Sentinel

Mpumalanga, near Lunsklip falls
KwaZulu-Natal, Karkloof
KwaZulu-Natal, Highmoor
Northern Cape, Nieuwoudtville
Western Cape, Vredenburg
Western Cape, near Darling
Western Cape, Caledon, Drayton
Western ا‎ Fairfield, Napier
Western Cape, near Matjesfontein
Northern Cape, near Springbok

el
Eastern Cape, Kologha Forest
KwaZulu-Natal, Inchanga
Northern Cape, Kamiesberg
Free State,
Northern Cape, near Middelpos

The Sentinel

Northern Cape, near Nieuwoudtville
Northern Cape, Hantamsberg
Western Cape, Piekeniers Kloof
Northern Cape, Oorlogskloof
Northern Cape, near Nieuwoudtville
Northern Cape, Papkuilsfontein south
of Nieuwoudtville
Northern Cape, Bokkeveld Mts.

Darling
Viljoen’s Pass

Rooisand, Bot River

Western Cape,
Western Cape,
Western Cape,
Northern Cape, near Nieuwoudtville
Free State, The Sentinel
Northern Cape, near Middelpos
Western Cape, Malmesbury
Northern Cape, near Nieuwoudtville
Northern Cape, near Nieuwoudtville
Free State, The Sentinel
Mpumalanga, Long Tom Pass
estern Cape, Malmesbury
Eastern Cape, Catheart district
Western Cape, Malmesbury
Northern Cape, G куз Farm

Eastern Cape, Naude's

Goldblatt & Manning 11070

Goldblatt & Nünni 11152
dblatt & Manning 11051
Goldblatt 72

Goldblatt s.n. no voucher

Goldblatt & Vann

Goldblatt & Manning 11084

Goldblatt т, еш 11096
Goldblatt
Goldblatt е Vom 10251
еге

adblatt j и 12086
595 It s.n. no voucher
Goldblatt & Porter 12007
Goldblatt & Nünni 11235
Goldblatt & Manning 9723
Goldblatt & Nanni 11232
Goldblatt 6067
Goldblatt 11403
Goldblatt & Manning 10043
Goldblatt & Nünni 11161

Goldblatt & Manning 9975
Goldblatt s.n. no voucher

Goldblatt 11102
Goldblatt 6272

Goldblatt & Nanni 11162

dblatt Nox 11052
Goldblatt 11157

Goldblatt s.n. no voucher
Goldblatt & Manni 11104A
Goldblatt & Nénni 11104
Goldblatt & Manning 9856
latt Ў 7 10480
Goldblatt
Goldblatt к as 12995
Goldblatt & Nünni 11087
Goldblatt 4035

Goldblatt & Manning 11067

Volume 91, Number 1 Goldblatt et al. 189
2004 Floral Biology of Hesperantha
50%) from five or more individuals per population, Manning (Diptera, Lepidoptera—butterflies), and

unless fewer individuals were available. Additional

nectar samples were dried on Whatman filter paper

van Wyk, Rand Afrikaans

no. | and sent to В.-К.

D Johannesburg. for HPLC nectar sugar

analysis.

INSECT OBSERVATION AND POLLEN LOAD ANALYSES

Behavior of insects on Hesperantha flowers was
carefully observed to see whether insects contacted
anthers and stigmas while foraging. Insects ob-
served probing the floral tube or brushing the an-
thers or stigmas were captured and killed in a jar
using ethyl acetate fumes. Pollen was removed from
insects after specimens were pinned. To prevent
contamination of the body of an insect with pollen
carried by another in the same jar. each insect was
wrapped in tissue as soon as it was immobilized by
jar fumes. Body length and. proboscis length of in-
sects was recorded from captured specimens.
Night-flying moths are difficult to capture simply
because darkness makes them difficult to locate.
Use of flashlights covered with translucent red cel-
lophane paper for illumination significantly assisted
observation and capture. Capturing some insects
(especially long-proboscid flies) at some sites ap-
peared to reduce the population significantly, so we
therefore killed as few of these insects as necessary
to obtain specimens for identification and. pollen
load analysis.

Removal of pollen from an insect involved gently
scraping pollen off the body with a dissecting nee-

Goldblatt et al., 1998a. b). The

from needle probes was collected on glass slides

dle (see € residue

and mounted in l to 2 drops of Calberla’s fluid
(Ogden et al..

flies, which are large insects, sites of pollen depo-

1974). In the case of long-proboscid

sition are often quite discrete for each plant visited,
and pollen species can often be identified without
recourse to microscopic examination due to pollen
coloration and position. Pollen grains were identi-
fied microscopically by comparison with a tempo-
rary reference set of pollen grain slides made from
plants flowering at study sites. Hesperantha pollen
grains are distinguished from co-blooming species,
other than members of Iridaceae subfamily Crocoi-
deae, by their large size. perforate-scabrate exine,
and monosulcate aperture with prominent 2-banded
1991).

identified by K.

operculum (Goldblatt et al.

Insect specimens were А
Dom-
D. Kroon,
Transvaal

E C.

Brooks. University of Kansas (Apidae). H.
brow, Worms. Germany (Scarabaeidae),
Sasolburg. South Africa, and H. Kruger.

Museum. Pretoria

(Lepidoptera—moths).

Kim E. Steiner, National Botanical Institute, Cape
Town (Mellittidae, Scarabaeidae). Voucher speci-
mens are deposited at the Snow Entomological Mu-
Kansas.

seum, Lawrence,

RESULTS

INFLORESCENCE
SPAN

PHENOLOGY AND FLORAL LIFE

Most Hesperantha species have an erect inflores-
cence reaching a height of 5-30 em. but a few spe-
cies of rocky habitats and cliffs. including H. brer-
and H.

stems and a nodding spike (Fig. 1). Individuals pro-

icaulis scopulosa, have weak. drooping
duce one or, in some species, two or more, simple

spicate inflorescences annually, and flowering is
closely synchronized within the same species or
population both seasonally and diurnally. Flower
buds are arranged more or less helically along the
spike (Goldblatt, 1984, 2003). In six species, in-
cluding H. flava, Н. humilis, and H. latifolia, the

lowering stem is mostly or entirely subterranean so

—

that the flowers are borne close to ground level (Fig.
IB). Flowering periods broadly subdivide into a
or October
in a few species) in the southern African winter-

spring season (August and September,

rainfall zone or a summer-autumn season (Decem-
ber to April) in the summer-rainfall zone (Table 2).
This coincides with the period of optimal plant
growth during or soon after the main rainy season
for the geographical area. A few species of the sum-
mer-rainfall zone flower in early to late spring (Hil-
liard & Burtt, 1986),

leaves have been produced, but for logistical rea-
| g

sometimes before foliage
sons we did not study these early flowering species.

The pattern of flower buds opening on an inflo-
rescence is acropetal. In all Hesperantha species a
mature flower expands and closes again within 12
hours at specific times characteristic of the species
or population. White, cream, or pale yellow flowers
of the southern African winter-rainfall zone are fra-
grant (Table 2) and typically open in the mid to late
afternoon or at sunset and close at specific times
in the night, always before daylight (Table 3). Flow-
ers of other colors, and white- to cream-flowered

species of the summer-rainfall zone, are scentless

—

Table 2) and open either in the early morning (H.
ciliolata, Н. pilosa blue-flowered form. as well as
most pink-flowered species of eastern southern Af-
rica) and close soon after midday, or open after the
middle of the day (H. pauciflora) and close before
sunset (Table 3). The red flowers of H. coccinea
open in the early morning and close shortly before
sunset. Examples of perianth color and form, re-

Annals of the
Missouri Botanical Garden

190

Table 2.

aeri tube include the wider upper portion that accommodates the head of a long-tongued insect; + = presence,

Floral characteristics of Hesperantha species arranged according to flower type. Measurements of the

e, trace = amount too little to measure volumetric ally; salver
Н. falo ata ane: H 4. pilosa are listed in the

— salverform. White-flowered nee eee of
first group, while yellow-flowered or blue-flowered populations respectively

are included in the second group. Examples: of del тои in Народ species are available in Manning et al.
I

(2002) and at http://www.mobot

df

Tube
Flower Flower length Flowering
Species shape color mm Scent Nectar time
Hesperantha falcata group
H. acuta salver white 8-11 yes + Aug.—Sep.
Н. bachmannii nodding tube white 8-10 yes + Aug.—Sep
H. cucullata salver white 7-9 yes + Aug.—Sep
Н. erecta salver white 8-10 yes + July-Sep
H. falcata salver white 7-9 yes + Aug.—Sep.
(also see below)
Н. flava tube-salver yellow 20-26 yes + June-July
H. flexuos salver white 7-9 yes + Aug.—Sep.
H. иек nodding tube white са. 12 yes + July—Aug.
H. pilosa (also see below) salver white 9-10 yes + Aug.—Sep.
H. pseudopilosa salver white 8-10 yes t ae —Sep.
Н. а salver hite ca. З yes trace Sep.
Н. radiat nodding tube white to cream 10-12 yes + ree —Sep.
Н. nili salver white 9-11 yes + Aug.—Sep.
H. s salver white 4—5 уез + Aug.—Oct.
Н. 4 salver yellow 12-16 yes + July-Aug.
Hesperantha pauciflora group
H. baurii salver pink 8-10 no trace Jan.-Feb.
H. ciliolata salver pink 5 yes + Sep.
Н. falcata salver vellow 7-8 no ? Aug.—Sep.
(also see above)

Н. fibrosa salver pink 7-9 no + Aug.—Sep.
H. humilis tube-salver pink 18-22 no = June-July
H. leucantha salver pale pin 10—15 по + Jan.—Feb.

salver creamy vellow 7-8 no + Jan.-Feb.
H. luticola tube-salver white with large dark 30—45 no trace July-Aug.

marks on the tepals

H. pauciflora salver pink to purple, or yellow 6-8 no trace or Aug.—Sep.
+

H. pilosa (also see above) salver blue 1-9 no + Aug.—Sep.

H. similis salver pink 1—5 по trace Jan.—Feb.

Hesperantha latifolia group

Н. brevicaulis tube-salver pink 22-30 no + Mar.—Apr.
coccine tube-salver red (or pink) (25-)30-38 no + Dec.—May

H. grandiflora tube-salvei pink, anthe rs brown 28-32 no + Jan.—Feb

1. huttoni tube-salver pale pink 22-35 no T Feb.—Mar.
latifo tube-salver р iie 20-27 no + Aug.—Sep

Н. oligantha tube-salver purple 25-35 no + Sep.

Н. pubinervia tube-salver uan -pink 20-25 no = Jan.-Feb.

H. scopulosa tube-salver pink 32-42 no = Feb.—Mar.

Н. stenosiphon tube-salver pink, anthers black 15-60 no + Feb.-Mar

H. woodii tube-salver pink 33—40 no # Feb.—Mar.

Hesperantha vaginata group

Н. vaginata cup yellow with brown 5-7 no = Aug.—Sep.

markings
Unplaced species
Н. pallescens tube-salver pale yellow 18-22 no + Sep.

Volume 91, Number 1 Goldblatt et al. 191
2004 Floral Biology of Hesperantha

Table 3. Contrasted timing of floral opening and closing in selected Hesperantha species. Only species for which
precise sud is available are included. and data are for study populations only (as in Table 1). Timing varies
within populations according to weather conditions, and other populations of the same species may have different
opening and closing patterns. Flowers of H. scopulosa do not fully close and have the ‘ents fully 3 for all
daylight hours and partially so at night. N/a = not assessed.

Species Opening Closing Days open

White-, cream-, or pale vellow-flowered species

Н. bachmannii 16:00-10:30 6:30-7:00 1
H. cucullata (15:00—)16:00—1060:30 (19:00—)20:00—20:30 n/a
H. erecta (14:00—)15:00—15:30 (17:00-)18:30-19:00 4-5
Н. falcata (12:30—)15:30—106:30 21:00-21:30 or 1-5
or 17:30-18:00 after 2:00
H. flava 16:00—17:00 n/a n/a
H. lactea 11:45-12:30 16:00-10:30 n/a
H. marlothii 17:00-17:30 1:00—4:30 n/a
Н. pallescens 8:00-8:30 18:30-19:00 n/a
H. pilosa (white-flowered) 17:30-18:00 3:30-4:30 |
H. pseudopilosa (15:00—)18:00— 18:30 after 0:00 n/a
H. erii 16:00-16:30 19:00-19:30 3-4
H. ra 18:00-18:30 5:30-6:30 0-7
ко 2 17:00-17:30 5:30-0:00 n/a
H. rivulicola 16:15-10:45 after 0:00 n/a
H. spicata 18:00-18:30 0:00-0:30 1—5
H. sufflava 15:30-16:00 after 0:30 1-5
Pink-. blue-. or deep vellow-flowered species
Н. baurit 7:30-8:00 11:30-12:00 3-4
or 11:00-11:30 or 16:30-17:00
H. brevicaulis ca. 11:00 n/a n/a
H. coccinea 7:30-8:00 18:00-19:00 3-4
H. humilis 8:00-9:00 16:00-16:30 n/a
H. oligantha n/a 14:00-14:30 n/a
H. pauciflora (13:00—) 1 4:00—1 4:30 17:00-17:30 n/a
Н. pilosa (blue-flowered) 8:30-9:00 12:30-13:00 n/a
Н. vaginata 14:30-15:00 16:30-17:00 n/a
H. woodii 9:00-9:30 14:00-14:30 n/a

produced in color, are available in Manning et al. days, flowers may not open completely for the entire
(2002). Representative photographs of Hesperantha day or the normal timing of opening may be delayed
flowers are also posted at the following URL to- until conditions are more favorable. The only ex-
gether with this article: кар чен mobot.org/ ception we have encountered is H. scopulosa, the

MOBOT/Research/Hespe pdf flowers of which do not close completely, but the

A flower typically lasts four din before collages tepals half close at sunset. and re-open fully to be-
of the perianth. but in a few species with a white come extended at 90° to the tube after 7:00 H the

perianth, flowers last six or seven days (e.g.. Hes- next morning.
perantha radiata, H. spicata), yet maintain the pat- Flowers of all species studied are weakly protan-

tern of opening and closing at specific times (Table drous. The anthers dehisce longitudinally within

3). Flower buds on the same inflorescence open one to three hours after the tepals of a new bud
sequentially, usually one day apart: hence, there first unfold, but this depends to some extent on
may be three or four flowers open at any time on ambient temperature and humidity (see above) and
an inflorescence for species with flowers lasting anthers dehisce later in the day under wet-cool
four days. but up to eight flowers open in species conditions, The three stylar arms. the adaxial sur-
in which flowers last six or seven days. When flow- faces of which comprise the stigmatic surfaces, are
ers close, the tepals cloak the anthers and stigmas held erect when the flower first opens but they di-
completely. Ambient temperature influences anthe- verge later during the same day. in most species
sis. On cold (< 15°C), heavily overcast, or misty spreading outward below the erect or divergent an-

192

Annals of the
Missouri Botanical Garden

thers, coming to lie over the extended tepals. In all
species the style divides at (or in a few species
below) the mouth of the perianth tube into three
long, slender arms (a generic synapomorphy for
1984, 2003) that ex-
tend between the filaments. Open flowers are typ-
ically held erect to suberect with the tepals spread-
ing horizontally with the stamens symmetrically
disposed.

Hesperantha, see Goldblatt,

Anthers are developmentally extrorse
with loculicidal dehiscence, and the pollen adheres
to the dehisced anther locules. The filaments twist
slightly in the open flower so that the anthers come
to face inward or upward, depending on whether
they are held erect (most species with colored te-
pals), or are articulated on the filaments, each one
lying horizontally, at right-angles to the filament
(crepuscular or nocturnal species with white or
cream tepals). Stamens and style branches аге
asymmetrically disposed and declinate in H. gran-
diflora, the only species in the genus with a zygo-
morphic flower.

Compatibility varies within the genus. Several
species have been reported to be self-compatible
(Goldblatt, 1984) following hand-mediated self-pol-
linations but with reduced fertility (Hesperantha
bachmannii, Н. cucullata, Н. falcata). Mechanical
autogamy without apparent reduction in fertility oc-
curred in H. acuta, Н. erecta, Н. latifolia, and H.
pallescens in the absence of pollinators. Hesperan-
tha pauciflora and Н. radiata failed to set seed fol-
lowing self-pollinations by hand. In the course of
the present study, self-compatibility was estab-
lished for H. quadrangula and confirmed for H. pal-
lescens (Goldblatt, 1984).

NECTAR

Nectar glands, when present (Table 4), are sep-

1, as they are in the entire subfamily Crocoideae
(Goldblatt. 1990, 1991; Goldblatt & Manning, un-
published). Nectar is secreted from three minute
pores at the top of the ovary (one per chamber)
directly into the base of the perianth tube where
the accumulated fluid is retained until removed by
a foraging insect. In species with the lower part of
the tube narrow and tightly enveloping the style, a
small amount of nectar may be present in the upper
part of the tube, presumably the result of capillary
action. Measurable volumes of nectar are produced
in most species (Table 4), and volume correlates
with tube length. The long-tubed flowers of Hesper-
antha coccinea (tube 25-38 mm long) and H. gran-
diflora (tube 28-32 mm long) produced the most
nectar (up to 4.1 pl in the latter in flowers undis-
turbed by insects—the perianth had not fully ex-

panded when nectar was measured), while flowers
of short-tubed H. baurii, H. falcata, H. fibrosa, H.
pilosa, H. quadrangula, and H. radiata produced
small amounts of measurable fluid (< 1.0 pl of
nectar). The smallest quantities of nectar are pro-
duced by Н. leucantha and H. baurii (less than 0.1
Ш in the last species). There is a negative corre-
ation between the percentage of sugar solute in
Hesperantha nectar and nectar volume. Thus, spe-
cies that secrete the greatest amount of fluid tend
to produce nectars lowest in dissolved sugars (e.g.,
H. brevicaulis, H. coccinea, H. grandiflora, and H.
woodii), while H. falcata, H. pilosa, H. radiata, and
H. spicata secrete less than 0.5 pl of fluid that con-
tains 35% to 48% dissolved sugars. Among species
that secrete less than 0.5 pl, H. bachmannii ap-
pears exceptional in having relatively dilute nectar,
with a mean of 21.

5% dissolved sugars.

Sugar analyses of Hesperantha flowers (Table 4)
indicate that species examined for sugar composi-
tion offer nectars that are sucrose rich. White-flow-
ered species with flowers open in the late afternoon
and evening, e.g., H. falcata, H. pilosa, H. radiata,
and H. spicata, have nectar of unusually high sugar
concentrations, 40-50%, while H. baurii has nectar
of 48% to > 50% sucrose equivalents. All the spe-
cies with white flowers so far examined secrete nec-
tar, although there are only trace amounts in H.
quadrangula, but nectar presence or absence varies
in species with flowers of other colors. The long-
tubed flowers of H. pubinervia and H. scopulosa pro-
duce no nectar at all.

FLORAL PRESENTATION AND POLLINATION SYSTEMS

Four overlapping pollination systems can be rec-
ognized in Hesperantha. Comparative floral traits of
the four main systems are summarized in Table 2.
The pollination systems and associated floral traits
do not necessarily reflect the natural re lationships
of species.

The Hesperantha falcata Group

In this group, of which Hesperantha falcata and
H. cucullata are typical examples, the flowers are
crepuscular or nocturnal and mostly white to cream
or exceptionally pale yellow, and the perianth is
salver-shaped with horizontally extended tepals
Figs.

—.

1A, 2A) or in three species, nodding (Figs.
1D, 2B) with lightly reflexed tepals (H. bachmannii,
H. marlothii, and H. radiata). The floral tube is
cylindrical, expanding slightly near the apex, and
hollow with a narrow, uniform diameter of about 1
mm. The tube typically contains nectar in the lower
1-3 mm. The perianth tube is usually slightly

Volume 91, Number 1
2004

Goldblatt et al. 193

Floral Biology of Hesperantha

Table 4. Nectar properties of Hesperantha species that produc e measurable quantities of nectar (see Table 2). SD

= standard deviation, (n) = number of individuals sampled, F
sugars were analyzed by B.-E. van Wyk (Rand Afrikaans University, Johannesburg, South Africa). Data marked with
from Johnson and Bond (1994). For H. acuta and one population of H. falcata, nectar from three flowers

an asterisk are

‘ru = fructose, Glu = glucose, n/a = not assessed. Nectar

was pooled to obtain sufficient nectar to register a refractometer reading.

Nectar (n) —
% Nectar sugars ucrose/
Hesperantha Mean % sucrose Glu + Fru
species Volume pl equivalents (25D) Fructose Glucose Sucrose (n)
Н. acuta 0.4—0.8 (3) т (poole d sample) n/a n/a n/a n/a
H. bachmannii 0.2—0.4 (8) 5 (2.6) n/: n/a n/a n/a
Н. baurú trace to 0.1 (6) me 50 n/a n/a n/a n/a
H. brevicaulis 1.0-1.6 (3) 19.3 (1.5) n/a n/a n/a n/a
Н. coccinea
site | 4—3.1 (5) 20.8 (1.6) n/a n/a n/a n/a
site 2 2.2-2.9 (10) 15.4 (0.9) n/a n/a n/a n/a
ite 3* 1.9 (19) 174 (n = 11) 42 13 15 0.18 (1)
H. cucullata 0.2—0.6 (8) 10.6 (3.7) n/a n/a n/a n/a
H. falcata
site | 0.3-0.5 (3) 32 (pooled sample) 39 38 23 0.27 (1)
site 2 0.2-0.5 (6) 36.2 (3.5) n/a n/a n/a n/a
ibrosa 0.3-0.4 (4) 21.3 (2.1) 24—25 15-28 17-61 1.17 (2)
Н. grandiflora 2.84.1 (5) 14.8 (1.0) n/a n/a n/a n/a
Н. huttonii 1.3-2.4 (8) 13.7 (1.6) n/a n/a n/a n/a
H. lacte 0.1—0.6 (10) 21.6 (3.0) n/a n/a n/a n/a
H. latifolia 0.7-1.1 (10) 28.5 (3.4) 2320 24-30 41-53 0.94 (3)
H. leucantha 0.4—1.0 (4) 16.8 (1.0) n/a n/a n/a n/a
Н. marlothii 1.4-2.2 (10) 35.9 (3.8) n/a n/a n/a n/a
H. oligantha 1.1-1.8 (5) 26.4 (3.9) 19-23 24-25 52-57 1.20 (2)
J. pallescens 0.8—1.2 (10) 35.5 (5.6) n/a n/a n/a n/a
H. pauciflora 0.1-0.5 (5) 35.4 (1.7) n/a n/a n/a n/a
(pink flowers)
(vellow flowers) 0.6—0.7 (10) 23.5 (2.4) n/a n/a n/a n/a
H. pilosa wed аш 0.2—0.4 (5) 14.2 (1.9) n/a n/a n/a n/a
(white flower 0.1—0.5 (10) 35.7 (3.5) n/a n/a n/a n/a
site 2 0.2-0.4 (3) 15.0 (6.1) n/a n/a n/a n/a
site 3 0.2—0.5 (6) 14.8 (2.7) n/a n/a n/a n/a
H. pse nes 0.2-0.5 (2) 42.0-48.5 n/a n/a n/a n/a
H. radia
site | 0.2—0.4 (2) n/a 1120 16-20 60-73 1.86 (3)
site 2 0.2—0.5 (3) 42.4 (3.9) n/a n/a n/a n/a
H. rivulicola 0.2-0.5 (3) 48.0 (2.0) n/a n/a n/a n/a
Н. spicata 0.2-0.5 (2) 42-45 n/a n/a n/a n/a
H. stenosiphon 4.2-6.5 (11) 17.5 (2.0) n/a n/a n/a n/a
H. sufflava 0.4—1.2 (10) 28.0 (2.6) n/a n/a n/a n/a
H. woodii 1.2-1.8 (5) 18.1 (0.9) n/a n/a n/a n/a
shorter than the tepals, thus 7-16 mm long (Table pauciflora is an exception. A rare, pale yellow-flow-

2) compared to tepals 12-16 mm long, but the tube
is half again as long as the tepals in H. flava, 20—
26 mm long, compared with tepals up to 16 mm
long.

Almost all white- to pale yellow-flowered species
of the southern African winter-rainfall zone are cre-
puscular or fully nocturnal (Table 3). The perianth
opens in the late afternoon, typically after 16:0
or at sunset, and closes before sunrise. Hesperantha

ered form of this otherwise pink-flowered species
(Goldblatt, 2003) has the tepals opening soon after
midday and closing before sunset. Hesperantha
quadrangula is unusual: its white flowers have an
unusually short perianth tube, 2-3 mm, compared
to the tepals, 9-12 mm long, and they open at ca.
16:00 H and close shortly after sunset but before
dark, ca. 19:00 H

. The widespread and common /.

falcata is notable for the varied times that flowers

194

Annals of the
Missouri Botanical Garden

ure |

of different populations open, some opening as ear-

ly as 16:00 Н, and others after 17:30 H. but in all

populations we examined, the flowers remain open

after 21:00 H
1

ca. 15:00 H

n H. erecta, the perianth opens at

The eastern southern African Hesperantha lac-

Growth forms and plant habit in Hesperantha. —A. Н.
l

el. acuta. —B. H. humilis. —C. H. oligantha. —D.
H. radiata. Scale bar = 10 mm for A, B, and D; 15 mm for C. (Drawn by Margo Branch, Cape Town.)

tea, H. hygrophila Hilliard & Burtt, H. inconspicua
(Schltr.) G. J. Lewis, and H. rupestris u. Вг. ex
R. С. Foster (the latter three not studied here) have
unscented, diurnal flowers with a white to cream
perianth that are open for only a portion of the day
and close fully before sunset, between midday and

Volume 91, Number 1
2004

Goldblatt et al.
Floral Biology of Hesperantha

195

Figure. 2. Perianth types in Ys 7 0 че —А. Н.

sufflava. —В. Н. radiata. —С.

| |

d^ /

H. oligantha. I). Н. coccinea.

—k. H. v eha Scale bar = . Shading code: dark stippling = purple (H. oligantha): light stippling = red
(H. coccinea): vertical hatching = ye "low: and aptid black = brown (H. vaginata). Drawn by John Manning.

late afternoon depending on the species (Hilliard
& Burtt, 1986: Goldblatt, 2003).

spects except perianth color they resemble more

Thus in all

closely species of the next group, the H. pauciflora
group.

When open. the flowers of species belonging to
the Hesperantha falcata group produce а strong.
sweet fragrance that is variable between, and some-
times within, species. Scents range from light rose
(Н. quadrangula, H. rivulicola) to jasmine or fran-
gipani (Plumeria) (Н. cucullata. H. falcata—some
populations: А. flexuosa. H. pilosa—some popula-
lions), narcissus (H. spicata), acrid-musk (H. erecta,
Н. falcata—some populations: Н. pilosa—some
populations: H. flava), or sweet with a strong
clove component 7 marlothii, Н. radiata).

Hesperantha Pup qe Н. pilosa, Н. quadran-
Н. rivulicola,

falcata are actively visited by large-bodied apid

gula, Н. sufflava, and sometimes V.

bees (Tables 5. 6) with probosces 3-10 mm long.
Bees forage for both pollen and nectar soon after

the flowers open in the late afternoon. The white
flowers are Conspicuous in the late afternoon light,
and Anthophora species or Apis mellifera can often
be seen visiting the flowers of these species. Small
settling nocturnal moths, mostly noctuids, and most
commonly Heliotis armigera, but also species of
Adelidae, Drepanogynidae, Geometridae, and Pyr-
alidae (Tables 5, 6), with probosces 4—12 mm long
are common and active at or after sunset and in
the early evening in the southern African winter-
rainfall zone, and regularly visit flowers of all the
species we observed for pollinators after sunset (H.
bachmanni, H. cucullata, Н. falcata, H. marlothii,

. pilosa, H. pseudospicata, H. radiata, and H. ri-
vulicola). Both bees and moths are polylectie for-
agers, and individual bees were found to carry the
pollen of co-blooming species (Table 6), including

196

Annals of the
Missouri Botanical Garden

Table 5

Length of mouth parts of insects captured on Hesperantha flowers, with perianth tube lengths. Measure-

ments are ranges for the insect or plant populations studied.

Mouth part
mm (n)

Insect species

Plants on which

Tube length
insect captured mm

Diptera

Prosoeca ganglbauri

27-30 (4) H. grandiflora, H. scopulosa 28—42
P. ganglbauri 28-32 (4) H. woodii 35-38
Р. peringuey 20-25 (3) Н. latifolia 15-25
P. sp. nov. 2 ca. 9 (2) H. pauciflora 6-8
Stenobasipteron wiedemannii 19-23 (3) H. huttonú 25-35
Hymenoptera
Amegilla capensis 9-10 (3) Н. baurii 8-10
Anthophora diversipes 6.5-8 (4) Н. cucullata, H. pauciflora, Н. pilosa, 6-12
1. rivulicola
Н. sufflava 12-16
Apis mellifera 3—4 (10) Н. baurti, Н. cucullata, Н. falcata 7-10
Lepidoptera [butterflies]
Aeropetes ca. 30 (1 H. coccinea 30-38
Papilio demodocus са. 25 (1) H. coccinea 30-38
P. nireus 22 (1) Н. coccinea 30-38
Lepidoptera [moths]
Agrotis segetum ca. 11 (1) H. rivulicola 8-11
Ceromitia sp. 11-12 (7) H. pseudopilosa, H. radiata, 8-12
H. rivulicola
Cucullia terensis ca. 12 (3) H. cucullata, H. pilosa 7-10
Drepanogynis sp. ca. 10 (1) H. rivulico 8-11
). dochmoleuca са. 7 (1) H. pilosa 9-10
D. rufigrisea ca. 11 (1) Н. bachmannii 8-10
Heliotis armigera 8-9 (6) H. bachmannii, Н. cucullata, Н. pseu- 8-12
dopilosa, H. r ta
Nomophila noctuella 5-7 (6) H. cucullata, H. aude Н. radi- 7-12
ata
Perizoma artifex ca. 4 (1) H. pilosa 9-10
Xylopteryx arcuata ca. 8 (2) H. cucullata 7-9

Bulbinella (Asphodelaceae), Lachenalia (Hyacin-
thaceae), Hermannia (Malvaceae), and Iridaceae
(including Gladiolus, Moraea) in their scopae or
corbiculae and/or on various parts of their bodies.
In contrast, only Hesperantha pollen was found on
the bodies of captured moths except for one visiting
Н. pilosa, but as there were no other obvious night-
flowering species at most of our study sites this is
not surprising

All moths captured while visiting Hesperantha
flowers settled on the inflorescence and crawled
over the flowers. They carried pollen on the under-
side of the wings, ventral part of the thorax, legs,
and sometimes on the antennae and proboscis. One
moth captured on Cyphia bulbosa (L.) P. J. Bergius
(Campanulaceae) at our Н. pilosa study site carried
pollen of that species as well as that of H. pilosa.
Pollen loads were light, often only a few grains be-
ing present. The bodies of moths are, however, poor

surfaces for carrying pollen, and it is not surprising
that after capture in a net and transfer to a killing
bottle very little pollen remained on their bodies by
the time they had been pinned and then examined.
Moth activity was found to be at a maximum for
the first hour and a half after sunset, thus until
about 20:30 H. After this we noted few, if any, moth
visits and we therefore did not continue our obser-
vations. It is possible that other moth species be-
come active later, as noted by Johnson et al. (1993)
for Crassula fascicularis Lam. (Crassulaceae), but
flowers of most crepuscular or nocturnal Hesper-
antha species close before 1:00 H, exceptions be-
ing Н. marlothii, Н. radiata, and Н. rivulicola, the
flowers of which remain open until dawn or day-

=

The pollination by small settling moths in Hes-
perantha follows the pattern described by Johnson
1997) for species of the orchid genus Satyrium.

Volume 91, Number 1
2004

Goldblatt 197

Floral ا‎ of Hesperantha

Johnson recorded a similar suite of moths visiting
different species of that genus at night: Heliotis ar-
migera and Syngrapha circumflexa on S. bicorne
(L.) Thunb. and Agrotis segetum on Satyrium ligu-
latum Lindl. and S. stenopetalum Lindl. with the
butterfly Vanessa сагаш also visiting S. ligulatum
during the day, a pattern paralleled in H. rivulicola.
A high nectar sugar concentration of 40.1% was
also noted for 5. stenopetalum, which is comparable
to the high nectar sugar concentrations we found in
most settling moth-pollinated species of Hesperan-
tha.

Those white-flowered species with flowers open-
ing at or after sunset, including Hesperantha flava,
H. marlothii, and Н. radiata, have not been seen
to be visited by bees. The long-tubed H. flava may
receive visits from sphinx moths according to Vogel
(1954), but while this is consistent with its long
perianth tube (18-28 mm long). we assume that
Vogel was only making a suggestion and did not
observe sphinx moths visiting the species. Among
the white-flowered species of the winter-rainfall
zone H, quadrangula is exceptional in having flow-
ers that close at about sunset, that is, before moths

are normally active. Thus, although it has white
flowers that open in the late afternoon, it 15 evi-

dently not pollinated by moths.

The Hesperantha pauciflora Group

The Hesperantha pauciflora group (Table 2) in-
cludes the common eastern southern African H.
baurii, its allies, H. lactea, H. leucantha, Н. similis,
and several more, the western Cape H. pauciflora,
and western Karoo H. humilis (Fig. 1B). The peri-
anth coloration is usually pink to purple, but blue
or mauve in some populations of H. pilosa and in
H. ciliolata, and cream to pale yellow in H. lactea.
Floral structure in this group is virtually identical
to that of the H. falcata group. but the flowers are
typically scentless (Table 2) and the tepals unfold
during the day, often in the morning, and close at
midday or shortly thereafter (H. baurii, H. pilosa—
blue form. H. similis), or in the early afternoon, then
closing by 17.30 H (H. pauciflora). Hesperantha cil-
iolata is exceptional in having fragrant flowers that
produce an unusual acrid, musky scent reminiscent
of that produced by some southern African species
of the orchid genera Corycium and Pterygodium,
and differing markedly from the sweet odors of spe-
cies of the H. falcata group. Flowers of the H. pau-
ciflora group produce small quantities of nectar,
mostly 0.1—0.3 pl in volume (Table 4). Flowers ac-
tively visited by bees may, however, contain no de-
tectable nectar when sampled in the field. When

sampled later, after placing cut stems in water over-
night, flowers yield nectar, indicating that visiting
insects may have removed all available nectar dur-
ing their foraging, or alternatively insufficient water
was available to plants to allow nectar production.

Species in this group are pollinated primarily by
large-bodied female anthophorine bees or worker
honey bees foraging for pollen or nectar, or for both
rewards. Bees land on the flower and brush both
the anthers and stigma lobes as they crawl over the
perianth while scraping pollen into their scopae or
corbiculae. Most apid bees, Amegilla, Anthophora,
and most Apis mellifera workers captured on Hes-
perantha flowers are polylectic foragers (Table ©),
and individuals were found to carry the pollen of
co-blooming Fabaceae, Asphodelaceae, Hyacintha-
ceae, Boraginaceae, and Iridaceae in their scopae
or corbiculae and on various parts of their bodies.
Perhaps significantly, however, almost half the Apis
mellifera workers captured, 11 out of 26 individu-
als, carried pure loads of Hesperantha pollen, in-
dicating temporary floral constancy, unlike other
bees analyzed for their pollen loads (Table 6). Flow-
ers of Н. pauciflora are occasionally also visited by
a relatively short-proboscid Prosoeca species, pres-
ently undescribed (Table 6), which behave much as
anthophorine bees in search of nectar.

Species of this group may also be visited by ho-
pliine beetles, but the significance of these beetles
compared to bees visiting the same species is dif-
ficult to assess. Hopliine beetles often visit a range
of plant species with the large. brightly colored
flowers that are particularly suited to their activities
Picker & Midgely, 1996; Goldblatt et al., 1998b).
which include assembly, competitive behavior, and
copulation. Nevertheless, it may be best to regard
species visited by both bees and hopliine beetles

—

as exploiting both groups of pollinators.

The Hesperantha latifolia Group (Table 2)

The Namaqualand and western Karoo species,
Hesperantha latifolia and Н. oligantha, and the
eastern southern African H. brevicaulis, H. gran-
diflora, Н. huttonii, Н. scopulosa. H. stenosiphon,
and Н. woodii exemplify the third pollination cat-
egory (Figs. 1C, 2C). In these species the flowers
are odorless. have an elongate perianth tube 20-60
mm long, and usually a pink to purple (rarely red)
perianth. The tepals are shorter than the tube,
mostly 15—25 mm long (exceptionally to 42 mm in
Н. scopulosa and to 38 mm in H. grandiflora), and
spread horizontally, or are slightly cupped in M.
stenosiphon and H. woodii. Exceptional in the group

and genus, H. grandiflora has the tube sharply bent

198 Annals of the
Missouri Botanical Garden

Table 6. Pollen load analysis of captured insects on Hesperantha species. Coleoptera: Scarabaeidae: Anisochelus,
Anisonyx, Clania. Hyme ae Apidae: Allodape, Amegilla, Anthophora, Apis. Colletidae: Scrapter. Halictidae: Patel-

lapis. Melittidae: Rediviva. Diptera: Nemestrinidae: Prosoeca, Stenobasipteron. Lepidoptera: Adelidae: Ceromitia. Dre-
و‎ DE Geometridae: Perizoma, Xylopteryx. Noctuidae: Agrotis, Cucullia, Heliotis. Nymphalidae:
. Pieridae: Papilio, Pyralidae: Nomophila. Satyridae: Aeropetes. Sphingidae. Hippotion. Data for Hesperantha

ralidae:
vaginata are from Goldblatt et al. (1998b) and those for H. latifolia are from Manning and Goldblatt (1996). Site

numbers refer to study sites as indicated in Table 1

Number of insects carrying pollen load(s)

Pollen from host

Plant and insect taxon Pollen from host flower alone flower plus other species
H. baurii
site 1
Amegilla capensis Y 0 3
Patellapis sp. Y 0 |
Rediviva пеш $ 0 6
hopliine beetle 1 0 |
e beetle 2! 3 3
site
Ден те 8 ra 5 0
Н. bachmannii
Drepanogynis rufigrisea | 0
Heliotis armigera l 0
unidentified noctuid moth | 0
Н. brevicaulis
Stenobasipteron wiedemannii not captured
Н. coccinea
site 2
Papilio nireus | 0
Papilio demodocus | 0
Site:
Aeropetes tulbaghia | 0
H. cucullata
Anthophora praecox. Y 0 |
А. schulzei 1 9 1 d 0 2
Apis mellifera 3 0
Cucullia terensis | 0
Heliotis armigera | 0
Nomophila noctuella 3 0
Xylopteryx arcuata 2 0
Н. erecta
Apis mellifera 0 5
Anthophora rufidicaudis 9 0 2
Н. falcata
site 1
Apis mellifera l 4
site 2
e incl. Heliotis armigera seen but not captured)
H. flexi
rete praecox $ 0 2
nellifera 0 2
H. grandiflora
Prosoeca ganglbauri 0 3
Н. huttonii
en wiedemannii’ 0 3
Н. lacte
Allodape stellarum $ 0 2
H. latifolia

Prosoeca peringueyi 0 1

Volume 91, Number 1
2004

Goldblatt et al. 199
Floral Biology of Hesperantha

Table 6. Continued.

Number of insects carrying pollen load(s)

ollen from host

Plant and insect taxon Pollen from host flower alone flower plus other species
. luticola
Apis mellifera 0 2
Н. marlothii
;uculia terensis | 0
(Hippotion celerio seen but not captured)
H. pauciflora (pink flowers)
site
Apis mellifera 0 1
site 2
Anisochelus inornatus' 2 2
Anthophora schulzei 9 0 2
Prosoeca sp. nov. 0 2
(vellow flowers)
Anisochelus inornatus 2 1
Anthophora diversipes $ 0 l
pis mellifera 2 0
H. dd. blue flowers)
Apis ifera 2 3
eke schulzei 9 0 l
Anthophora krugeri 0 l
Anthophora diversipes $
(white fle 0 l
Anthophora rufidicaudis 9 0 2
Cucullia terensis 2 0
Drepanogynis dochmoleuca | 0 (1 with no pollen)
Perizoma artifex |
H. pseudopilosa
Ceromitia sp. 2 0
Drepanogynis е 1 0 (1 with no pollen)
Heliotis armig 1 0 (5 with no pollen)
Heliotis sc а l
Nomophila noctuella і 0 (2 with no pollen)
(Hippotion celerio was captured but did not contact style branches or anthers and carried no Hesperantha pollen)
H. quadrangula
Apis mellifera 0 2
Anthophora diversipes $ 0 2
Scrapter sp. indet. $ 0 |
Anisonyx ignitus 0 |
Н. radiata
Ceromitia sp 2 0
Heliotis armigera 1 0
Nomophila noctuella 1 0
H. rivulicola
Anthophora diversipes Y 0 |
Agrotis segetum l 0
Ceromitia sp. 3 O (1 with no pollen)
0

Drepanogynis sp
(Vanessa cardui was not captured but individuals were sec
H. scopulosa
Prosoeca ganglbauri
H. similis
Amegilla capensis Y
H. stenosiphon
Apis mellifera'

n to contact anthers and style branches on visits)

0 3
0 2
3 А

200

Annals

of the
Missouri Botanical Garden

Continued.

Table 6.

Number of insects carrying pollen load(s)

Plant and insect taxon

Pollen from host flower alone

Pollen from host
flower plus other species

Н. sufflar
Apis mellifera 0
Anthophora 8 9 0
— а kru d 0
Anisonyx ditu 0
Scrapter sp. nov. 9 0
Scrapter aff. m 9 0
Н. vaginate
Лата m 7
Н. woodii
Prosoeca ganglbauri 2
Total 74

105

' = more individuals seen but not captured.
8b).

? — Lepisia sp. of Goldblatt et al. (199.

near the apex so that the flowers face to the side,
with the tepals held more or less vertically. The
stamens and style branches of this species are uni-
lateral with the anthers and style arms arching
downward. Flowers of the H. latifolia group typi-
cally produce relatively large quantities of nectar
(Table 4), mostly 1—4 pl in volume with concentra-
tions ranging from 14.8 to 28.5% sucrose equiva-
lents. Eastern southern African species have un-
usually low nectar concentrations, less than 21%
sucrose equivalents and with a mean as low as
14.8% in Н. grandiflora and 13.7% in Н. huttonii.
The flowers of H. scopulosa lack nectar, as do those
of H. pubinervia (for which we have no pollinator
observations). The long-tubed flowers of the rare H.
pubinervia have an unusually narrow tube (Gold-
blatt, 2003), which may not accommodate the pro-
boscis of a long-proboscid fly.

Flowers of most species in the Hesperantha la-
tifolia group are visited and pollinated exclusively
by long-proboscid flies in the family Nemestrinidae.
In the southern. African. winter-rainfall zone, the
long-tubed H. latifolia is pollinated by the nemes-
trinid Prosoeca peringueyi, while H. oligantha and
H. purpurea are inferred to be pollinated by a sec-
ond and undescribed Prosoeca species, P. sp. no
(see Goldblatt et al., 1995; Manning & Goldblatt,

1996). Long-tubed species of the summer-rainfall
zone, including H. grandiflora, H. scopulosa, and
Н. woodii, are pollinated by P. ganglbauri, while
Н. brevicaulis and Н. huttonii are pollinated by
The elongated. pro-

z

Stenobasipteron wiedemannii.
bosces of these flies are typically slightly shorter
than the length of the perianth tubes of the Hes-
perantha species that they visit (Table 5), but these

flies are the only insects that are able to forage on
the nectar held in the lower part of the perianth
tube. While flowers of H. stenosiphon seem obvi-
ously adapted for long-proboscid fly pollination, we
found no flies at our study site; instead, honeybees
were visiting the flowers and collecting pollen. In
doing so they were seen transporting pollen from
anthers of one plant to style branches of another,
effecting pollination.

An important exception in the Hesperantha la-
tifolia group is the red-flowered form of the riverine
species H. coccinea (Fig. 2D). This plant has two
color morphs, the more common red-flowered form
pollinated by a guild of large butterflies including
Aeropetes tulbaghia (Satyridae) and Papilio species
(Papilionidae). Visits by Aeropetes have also been
reported by Johnson and Bond Johnson
(pers. comm.) has also seen an unidentified long-
proboscid fly visiting the red-flowered form, but this
has been witnessed only once to date. The second
color form of H. coccinea has a pink perianth. We
have no observations on visitors to the pink form.
Its pink perianth may indicate a dependence on
long proboscid flies for pollination. Because only
one color form of one species of Hesperantha is
pollinated by large butterflies, it seems unreason-
able to recognize an additional pollination group in
the genus.

Flies grasp the tepals with their tarsi and probe
for nectar while continuing to vibrate their wings,
contacting anthers and stigmas with the ventral or
lateral parts of the head and thorax. In the case of
Hesperantha grandiflora, pollen deposition is al-
ways on the ventral part of the thorax because the
unilateral stamens are positioned below the mouth

Volume 91, Number 1

Goldblatt et al.
Floral Biology of Hesperantha

of the floral tube. Field observations and pollen
load analyses show that all fly species visit open
flowers of other species during foraging bouts and
that most of these species have morphologically
convergent flowers that may be regarded as belong-
ing to specific pollination guilds. Thus. Prosoeca
peringueyi visits a range of plants with intense red
or violet flowers, including Pelargonium magen-
teum J. J. A. van der Walt (Geraniaceae) and spe-
cies of Iridaceae such as Babiana curviscapa G. J.
Lewis, В. dregei Baker, and Lapeirousia silenoides
(Jacq.) Ker Gawl. (Manning & Goldblatt, 1996), as
well as H. latifolia in the Kamiesberg of Namaqua-
land. Likewise, Prosoeca ganglbauri visits several
pink-flowered species including Gladiolus micro-
carpus С. J. Lewis (Iridaceae), Nerine bowdenii S.
Watson (A vIli
siphon (Kuntze) K. Schum. (Scrophulariaceae) dur-

eae), and Zaluzianskya micro-

ing foraging bouts on H. grandiflora or H. scopulosa
in the northern Drakensberg.

The Western Cape Hesperantha pallescens is ex-
ceptional in having pale yellow flowers with an
elongate perianth tube with the flowers opening
soon after sunrise and closing before sunset. The
flowers conform to the model for species pollinated
by another long-proboscid fly, Philoliche (Tabani-
dae) (Goldblatt et al., 1995; Goldblatt & Manning.
2000). To date we have not located a study popu-
lation at an undisturbed site where the predicted
pollinator is active, and we have seen no insect
visitors to the species at our study site during ap-
parently ideal conditions for insect activity,

Two patterns of butterfly behavior can result in
pollen dispersal and pollen deposition. The first has
been described as "inspection visitation" by John-
son and Bond (1994). A butterfly making an in-
spection visit does not land or feed on a flower, but
its comparatively long body and broad wings often
brush against the anthers and long style branches
or stigmas as it swoops close to an open flower be-
fore moving to another, sometimes of the same spe-
cies. In contrast, a true foraging visit requires that
the butterfly actually grasp the tepals and insert its
proboscis into the floral tube. In doing so. the ven-
tral surface of the thorax and. proximal abdomen
become dusted with pollen. Butterflies noted and
captured visiting red-flowered Hesperantha cocci-
nea include Papilio demodocus, P. nereis, and Aero-
petes tulbaghia, the latter also reported by Johnson
and Bond (1994) to be a pollinator of this plant.

The Hesperantha vaginata Group

The Hesperantha vaginata group (Table 2) in-
cludes only H. vaginata and H. karooica Goldblatt

(not studied), which have unscented, bright yellow
flowers, often marked with bold splashes of con-
trasting dark brown color (Fig. 2E). These flowers
have a relatively short tube, 5—8 mm long, that pro-
duces no measurable nectar. The tepals, 30-35 mm
long, much exceed the length of the tube. These
flowers open during the middle part of the day, 13:
00 H in H. vaginata, and close in the late after-
18:00 H in warm weather.

Hesperantha vaginata is visited exclusively by

noon, ca

the hopliine beetle Clania glenlyonensis (identified
1998b) (Table

6). The flowers have the stereotyped adaptations for

as Lepisia sp. 1 in Goldblatt et al..

the hopliine beetle pollination system, a large flow-
er with spreading or somewhat cupped tepals, re-
duced perianth tube, absence of nectar, and bold
contrasting. pigmentation (so-called beetle marks)
(Picker & Midgley, 1996; Goldblatt et al., 1998b:
Steiner, 1998). Clania individuals spend a consid-
erable time in a flower, either crawling about or at
rest with their heads pointed toward the center for
up to 20 minutes. Sometimes their visits may last
much longer, and beetles may even spend the night
in the closed flowers. Hopliine beetles use the flow-
ers of H. vaginata and some other species growing
nearby. including Romulea monadelpha (Sweet)
Baker (Iridaceae)
ceae). as sites for assembly, intraspecific competi-

and Arctotis acaulis l. (Astera-

tion, and mating. They are invariably covered with
a combination of pollen of H. vaginata and the co-
blooming species listed above. Although these bee-

tles feed on pollen and sometimes on tepal tissue,

they do little or no damage to flowers (Steiner.
1998: Goldblatt et al.. 1998b)

DISCUSSION

Pollination biology varies among Hesperantha
species but correlates closely with the mode of flo-
ral presentation, timing of anthesis, and nectar se-
cretion. Contrary to past predictions (Scott Elliot.

891: Marloth, 1915: Vogel, 1954). white-flowered
species that have flowers opening in the late after-
noon and remaining open at night are not exclu-
sively pollinated by moths. Indeed, our studies of
the floral biology of Hesperantha, incomplete as
they are, highlight the danger of inferring the pol-
lination systems of plants with limited fieldwork or
entirely from floral. morphology. Marloth (1915:
plate 42) suggested the genus was primarily polli-
nated by moths, based on his observation of small
moths (not identified) seen visiting H. falcata. Vogel
(1954) carried this further in suggesting that long-
tubed species including H. flava, H. grandiflora, H.
longituba (by which he probably meant H. huttonii).

202

Annals of the
Missouri Botanical Garden

and H. pulchra were pollinated by sphinx moths.
The last three species have odorless, pink flowers
that close at night. Vogel also speculated that the
yellow and brown, short-tubed flowers of H. vagin-
ata (which he knew as Н. metelerkampiae) and the
pink-flowered H. pauciflora were pollinated by bees
(Vogel, 1954: 103). He was partly correct only in
his assessment of H. pauciflora, and possibly of H.
Лага, for which we await field observations.

At first glance the adaptive radiation of pollina-
tion systems in Hesperantha parallels that found in
larger genera of the Iridaceae in southern Africa,
but with an unusual emphasis on white flowers
opening in the late afternoon or evening, a pattern
best developed in the southern African winter-rain-
fall zone. Specifically, Bernhardt and Goldblatt
(2000) noted the number of pollination systems in
an African genus of the Iridaceae correlates posi-
tively with the number of species in the genus.
Genera containing more than 100 species (e.g..
Gladiolus and Moraea) have the most diverse pol-
lination systems exploiting up to eight broad cate-
gories of pollen vectors. With the exception of Fer-
raria (са. 12 species) and Sparaxis (15 species).
genera of Iridaceae with less than 20 species (e.g..
Micranthus, Nivenia) do not have more than two
modes of animal pollination (Goldblatt et al.,
2000a; Bernhardt & Goldblatt, 2000; unpublished
data). Hesperantha, with 79 species, Geissorhiza (85

—

Spb. ), Ixia (ca. 50 spp.). and Lapeirousia (40 spp.
each have four or five major pollination modes
(Goldblatt et al., 1995, 2000b; Bernhardt & Gold-
blatt, 2000).

Four major modes of pollination (bee and cre-
puscular settling moth: diurnal bee: hopliine beetle:
long-proboscid fly, or large butterfly) are confirmed
for Hesperantha based on our field observations and
collection of floral foragers with analysis of their
pollen loads. A fifth mode of pollination by sphin-
gid moths, predicted by Vogel (1954) for H. flava,
remains to be confirmed by future field investiga-
tion.

Furthermore, pollination systems in Hesperantha
also subdivide along predictable modes of floral
presentation already described in other genera of
Iridaceae. This is most striking in the A. latifolia
group where tubular, odorless flowers with different
patterns of floral pigmentation are pollinated by dif-
ferent genera or species of two families of long-
proboscid flies. As described in the genera Babi-
ana, Gladiolus, and Lapeirousia, tubular flowers
that are pink to the human eye (e.g.. H. brevicaulis.
Н. grandiflora, H. huttonii, H. woodii) are most
likely to be pollinated by the Nemestrinidae Pro-
soeca ganglbauri and Stenobasipteron wiedemannii.

In contrast, those with intense blue to purple flow-
ers (e.g.. H. latifolia, Н. oligantha) are pollinated
by Prosoeca peringueyi or an undescribed Prosocea
species. Pale yellow to cream, tubular flowers are
more likely to be pollinated by long-proboscid ta-
banids in the genus Philoliche (Goldblatt et al.,
1995; Goldblatt & Manning, 2000; Manning &
Goldblatt, 1996, 1997).

UNIQUE TRENDS IN THE FLORAL ECOLOGY OF
HESPERANTHA

Pollination systems incorporating. large-bodied
bees, long-proboscid flies, or hopliine scarab bee-
tles have been well described in 14 other genera
of the Iridaceae of southern Africa and are not in

^
ш

any manner unusual in Hesperantha (Bernhardt &
Goldblatt, 2000). There are, however, two modes of
pollination in this genus atypical of the family.
First, pollination by deceit is suggested in the tu-
bular, pink flowers of H. pubinervia and Н. scopu-
losa. While both species have the pigmentation and
floral tube length of nectariferous species pollinated
by long-proboscid flies, both fail to secrete nectar.
As this mode of floral presentation is virtually iden-
tical in co-blooming species pollinated by the same
flies. H. pubinervia and H. scopulosa evidently rep-
resent either Batesian or guild mimics. These two
modes of deceit are more common in the Orchi-
daceae (Dafni & Bernhardt, 1989), including the
southern African genus Disa (Johnson, 1994; John-
son et al., 1998). Second, our documentation of pol-
lination mechanisms in the Hesperantha falcata
group is the first record in the Iridaceae of species
either exploiting both settling moths of five lepi-
dopteran families with crepuscular to nocturnal for-
aging habits and large-bodied apid bees (Antho-
phora and Apis), or settling moths alone. While
generalist pollination systems combining bees and
Lepidoptera have been described in a few species
of Lapeirousia (Goldblatt et al., 1995), these species
depend on true butterflies and sometimes moths
with diurnal habits. In contrast, full floral presen-

—

ation by species of the H. falcata group begins at
twilight. Thus, while several species of the H. fal-
cata group attract large-bodied bees, Gladiolus and
Lapeirousia species receive the majority of their
visits from bee pollinators from mid morning to ear-
ly afternoon, and their flowers often close at night.
Bee pollination in the H. falcata group only begins
at the end of the day, and flowers remain open after
sunset to exploit a second group of pollinators that
belong to another order of insects.

Other genera of the African Iridaceae in which
moth pollination is known or inferred, Babiana (un-

Volume 91, Number 1
2004

Goldblatt et al.
Floral Biology of Hesperantha

published data), Gladiolus (Goldblatt et al.. 2001:
Goldblatt & Manning, 2002). and Lapeirousia
(Goldblatt et al.. 1995), have larger flowers with a

relatively long perianth tube, and are visited either

by hovering sphinx or noctuid moths with long pro-
bosces. The foraging pattern in these species is un-
like that shown by small moths on Hesperantha
flowers, in which individuals crawl over the inflo-
rescence, visiting one flower after another before
moving to another plant.

The dark red or brown pigmentation on the re-
verse of the outer tepals of most otherwise white-
flowered species of the Hesperantha falcata group
may be a form of crypsis. When the perianth is
closed, only the outside of the outer tepals is visi-
ble. and the dark color presumably camouflages the
perianth from both herbivorous beetles and nectar-
robbing bees. Johnson (1995) postulated a similar
reason for the dark red color of the orchid Disa
(Monadenia) ophyridea (Lindl.) Bolus. which is also
pollinated by noctuid moths. These flowers cannot
close fully, hence the heightened need for cryptic
coloration to prevent nectar and pollen robbers. In
this species moths evidently locate flowers solely
by olfactory cues.

At first glance. butterfly pollination in Hesper-
antha coccinea appears to converge with the Aero-
petes tulbaghia pollination system described by
Johnson and Bond (1994). These authors have de-
scribed a true guild of red-flowered species that
bloom primarily in the southern African winter-
rainfall zone and are pollinated almost exclusively
by the large satyrid butterfly A. tulbaghia. This
guild includes several species in the Amaryllida-

ceae and Iridaceae and is characterized by the

arge, bright red flowers, sometimes with white nec-
tar guides, relatively narrow floral tubes and ample.
but relatively dilute nectar. Although it occurs in
the southern African summer-rainfall zone, Hesper-
antha coccinea appears to fit this profile. but more
important, it is not pollinated exclusively by Aero-
petes. unlike the guild of large butterfly flowers in
the winter-rainfall zone. The pollination system of
H. coccinea also incorporates some of the larger
species of butterflies in the family Papilionidae.
Thus even though Aeropetes has a strong. innate
attraction for red flowers. it is not the only visitor
to red butterfly flowers in southern Africa. The lack
of pollination by other large butterflies in the win-
ter-rainfall zone may simply reflect. the seasonal
searcity of other large butterflies there. We note that
other large butterfly flowers of the summer-rainfall
zone include red-flowered species such as Bauhi-
nia galpinii N. E. Br. (Fabaceae). Gloriosa superba

„ (Colehicaceae). as well as those of other colors

such as blue-flowered Plumbago auriculata Lam.
(Plumbaginaceae). In eastern southern Africa Aero-
petes seems to have a weaker affinity for red flowers
and often visits yellow flowers of Kniphofia (Aspho-
delaceae). in addition to the red flowers of plants
such as Gladiolus saundersii J. D. Hook. (Goldblatt
& Manning, 2000, 2002) as well as H. coccinea. It
is unlikely that red pigmentation and tubular flow-
ers limit the access of large butterflies other than
А. tulbaghia in the classic definition of butterfly
pollination (Faegri & van der Pijl, 1979). in which
red pigmentation and a narrow floral tube are rel-

atively common.

POLLINATION SHIFTS IN HESPERANTHA

With the exception of species of the Hesperantha

falcata group, pollination systems in this genus re-

flect the exploitation of the usual range of southern
the

n contrast to other genera of Iridaceae.

Mrican insects responsible for pollination и

=

family.
however, we also note that minimal shifts in floral
characters are all that has been required to change
a pollination system.

In particular, the morphological modification of
Hesperantha flowers has been limited to the length
of the perianth tube and the orientation of the te-
pals at anthesis. This conservative trend must be
compared to the shifts in the pollinations systems
of Moraea requiring severe changes in tepal ori-
entation and differentiation of the inner and outer
tepals and in the morphology of the staminal col-
umn and style branches (Goldblatt & Bernhardt.
1999). We must also compare the relatively con-
servalive perianth morphology of. Hesperantha with
that of Gladiolus in which floral symmetry and floral
tube shape and orientation change with the primary
pollinators (Goldblatt & Manning. 1998: Goldblatt
et al., 1998a). Instead, significant alterations of flo-
ral presentation in Hesperantha are limited to rel-
atively minor shifts in floral pigmentation, correlat-
ed with variation in scent production and nectar
secretion. Indeed, to the human eye Hesperantha
flowers appear to lack the unusually complex. con-
trasting patterning of pigmentation typical of the
flowers of most other genera of the family in south-
ern Africa.

Comparatively minor differences in nectar sugar
composition and concentration have had a dramatic
effect on which insects are most likely to pollinate
a Hesperantha flower, for the important reason that
these biochemical characters evolved in association
with shifts in the mechanics of floral. phenology.
Specifically, the stereotyped opening and closing of

tepals in different species. at different seasons, and

204

Annals of the
Missouri Botanical Garden

at different times of the same day sharply restricts
foraging by prospective pollinators. Mature flowers
that remain closed while particular species of an-
thophilous insects are actively searching for edible
rewards are almost as effectively excluded from de-
veloping novel interactions as they would be if they
bloomed at a time of the year when the same insects
are absent.

A change in pollinator from an insect with rel-
atively short mouth parts, such as apid bees, short-
proboscid nemestrinids, small moths, and possibly
other polyphagic taxa, to one with longer mouth
parts, such as long-proboscid nemestrinids, may
seem a relatively moderate shift and merely one of
degree. It must, however, be remembered that a
shift to a long-proboscid fly pollinator means a
change from a system where several species of bee
and fly, or several different species of moth, may
pollinate a species to one where only a single spe-
cies is the primary or sole pollinator. Long-probos-
cid flies are particularly effective pollinators of cer-
tain plants because relatively few plants offer them
a reliable source of nectar, and they usually carry
heavy loads of pollen on specific parts of their bod-
ies, limiting or avoiding stigma clogging (Goldblatt
& Manning, 2000).

however, visit many species, sometimes in a non-

The shorter-tongued insects,

constant pattern, and they usually mixed

loads of pollen that are often randomly scattered

carry

over their bodies. These contrasting patterns of pol-
lination must have important consequences for the
reproductive systems of the two plant groups. A
shift to a specialist pollination system using just
one pollinator species presumably has important
consequences for the radiation of a genus despite
the apparently trivial shift in morphology and phys-
iology.
DISTRIBUTION OF POLLINATION SYSTEMS
In the absence of any phylogenetic hypotheses
about the radiation of Hesperantha, the origin and
evolution of pollination systems in the genus re-

mains a speculative topic. Small white, crepuscular

or nocturnal flowers are unknown in subfamily Cro-
coideae outside the genus, and this pollination sys-
tem must be derived. Flowers in Geissorhiza, the
genus to which Hesperantha is most closely related
(Lewis, 1954; Goldblatt, 1984; Reeves et al., 2001),
may be pink, blue, violet, or white, but are always
diurnal. The most common, and presumably ances-
tral pollination system in Geissorhiza is a general-
ized one (Nänni, unpublished data) in which the
small, short-tubed flowers are open during the day
and offer both pollen and small quantities of nectar.

They are visited by a range of insects including
Apis mellifera, hopliine beetles, butterflies, bee flies
(Bombyliidae), and short-proboscid tabanid and ne-
mestrinid flies, and these species may be consid-
ered generalists. The pollination system in Hesper-
antha that most closely resembles this system is
the large-bodied Apis mellifera—anthophorine bee,
hopliine beetle, and short-proboscid nemestrinid fly
system found in the winter-rainfall zone H. pauci-

flora, and the anthophorine bee system in such

eastern southern African species as H. baurii, H.
lactea, and H. similis.

The long-proboscid fly pollination system in Hes-
perantha is, we assume, derived, since it is a more
specialized system than those using a wider range
of pollinators. The taxonomic distribution of the
strategy in the genus makes it clear that it has had
2003). The eastern
southern African species pollinated by Prosoeca

multiple origins (Goldblatt,

ganglbauri or Stenobasipteron wiedemannii may
share a common ancestry. However, the Namaqua-
land H. latifolia, pollinated by Prosoeca peringueyi,
and the western Karoo H. oligantha, inferred to be
pollinated by an undescribed Prosoeca species, be-
long to different taxonomic sections of Hesperantha
(according to Goldblatt, 1984, 2003). Long-probos-
cid fly pollination is also inferred for two apparently
unrelated species of Hesperantha sect. Radiata, the
eastern Cedarberg H. elsiae and the southern Cape
Н. muirii, based on flowers with an elongate peri-
anth tube and pink coloration. These two species
are most likely local derivatives of the widespread
H. radiata, the nocturnal flowers of which are pol-
linated by moths. Thus, while we can say little
about the origins of moth pollination in Hesperantha
flowers, it is clear that long-proboscid fly pollina-
tion evolved several times in the genus and involves
different species of nemestrinid (and possibly ta-
banid) flies across the range of the genus in south-
ern Africa. This mirrors the pattern in Gladiolus
(also belonging to the Crocoideae), in which long-
proboscid fly pollination may have evolved at least
10 and possibly 12 times in this genus of 165 spe-
cies in. southern. Africa (Goldblatt & Manning,
1999; Goldblatt et al., 2001).

The shift to butterfly pollination in red-flowered
populations of Hesperantha coccinea is unique in
the genus. Although butterflies may share this riv-
erine species with long-proboscid flies, it seems
likely that only the rare pink-flowered populations,
which Occam's razor suggests must be ancestral,
are normally pollinated by long-proboscid flies. The
red-flowered populations, which extend from the
Amatola Mountains in Eastern Cape Province,
South Africa, to Zimbabwe, are pollinated largely,

Volume 91, Number 1
2004

Goldblatt et al.
Floral Biology of Hesperantha

if not exclusively, by a range of large butterflies,
including species of Papilionidae and the satyrid
Aeropetes.

The shift to exclusive hopliine beetle pollination
in Hesperantha vaginata (and perhaps its close ally
H. karooica) is likewise unique in the genus, but
flowers shared by apid and anthophorine bees and
hopliines occur in a few other species of Hesper-
antha, notably H. pauciflora. The evolution of a
strictly hopliine pollination system is thus not par-
ticularly surprising.

In summary, the radiation of pollination systems
in Hesperantha, a mid-sized genus of subfamily
Crocoideae of the Iridaceae, is not unexpected in
view of the diversity of pollination systems in most
other genera of any size in the subfamily. Each ge-
nus. however. appears to exploit the available spec-
trum of pollinators in different ways and to different
degrees. Ixia exhibits a remarkable pattern of ra-
diation based on hopliine beetle pollination and
secondarily on long-proboscid flies. whereas Glad-
iolus exploits in particular anthophorine bee polli-
nation, with secondary emphasis on long-proboscid
flies. Lepidoptera, or passerine birds. Lapetrousta
has exploited a range of different long-proboscid
flies as pollinators, while a few species have flowers
adapted for sphinx or other moth pollination, but
some species are pollinated by a combination of
bees. wasps, and butterflies.

The pattern of radiation in Hesperantha shows
particularly marked exploitation of long-proboscid
fly pollination in eastern southern Africa, where 11
of the 34 species there (Goldblatt, 2003) have flow-
ers that display the typical adaptations for this
strategy. In contrast, species of the southern Africa
winter-rainfall zone have exploited small moth pol-
lination (or a combination of moths and apid and
anthophorine bees) at the expense of most other
pollination systems. Hopliine beetle, exclusive an-
thophorine bee, and long-proboscid fly systems are
limited to only a few species there. Some 22 of the
44 species in the winter-rainfall zone have been
shown herein, or may confidently be inferred, to
have this small settling moth pollination system,
often associated with foraging by large anthophor-
ine bees late in the day, a system not otherwise

known in the Iridaceae.

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LINEAGE SORTING AND Tzen-Yuh Chiang,?? Kuo-Hsing Hung.“
PHYLOGEOGRAPHY IN Tsai-Wen Hsu," and Wen-Luan Wu”
LITHOCARPUS FORMOSANUS

AND L. DODONAEIFOLIUS

(FAGACEAE) FROM TAIWAN!

ABSTRACT

Gene genealogy of the cpDNA atpB-rbel, noncoding spacer was reconstruc led to assess the phyloge napi pattern
of two c donc и d oaks. Lithocarpus Jormosanus (Skan) Hayata and £. dodonaeifolius (Hayata) Hayata (Fagaceae).
High levels of nuc 1 und haplotype ‹ iversities but low levels of genetic differentiation between spe cies and among
populations were detected. The result is consistent with the paraphyly of this epDNA spacer in both species ا‎
bv a neighbor-joining analysis. A minimum spanning nelwork of the cpDNA haplotype s identified ч, major clades.
and A' (consisting of clades of B. C. and D). No clades were confined to either species or single populations. C E. "s

B and C did not occur in two smaller и of L. dodonae áfolius. The apportionment of haploty pes between specie
аці populations indicated a lineage sorting of the ер) noncoding spacer. On the contrary. RAPD 5

revealed limited ongoing gene flow and significant genetic differentiation between species and among populations.
Given low possibilities that seeds disperse across a lang veographic range in the modern vege n high Vm values
estimates of number of migrants per generation deduced from the seed-carried organelle DNA marker are likely to
represent historical migrations. A migrant-pool model explains the 5 ee p- the organelle DNA
within populations and the low differentiation among populations. According to geological evidence, during the degla-
ciation period common ancestral populations were possibly forced to migrate into re fugia at local peaks. Invading and
adapting to habitats of different elevations. two oaks flower with a lag interval of about half a month, which may have
triggered the reproductive isolation and speciation. Ancestral polymorphic alleles, however, prolonged the lineage sorting
period within populations and species. Given a relatively short evolutionary duration since isolation, high genetic

5

heterogeneity has made the attainment of coalescence improb: able
Key words: Fagaceae, lineage sorting, Lithocarpus, phy loge em Taiwan.

One of the recent developments in plant evolu- cies. In contrast to the distinctness between species
tionary study is the application of phylogeography descending from remote common ancestors (е...

to the analysis of evolutionary events (cf. Avise, Quercus sects. Lobatae and Cerris, Manos et al.,

1999). Phvlogeography uses gene 5 1999), low genetic differentiation of organelle
which trace phylogenetic relationships among al- DNAs between closely related species has been fre-
leles within or among species, in a geographical quently encountered (e.g... /«pomopsis. Wolf et аһ,
context (Schaal, 2000). In the past, phylogeograph- 1997: Quercus, Dumolin-Lapegue et al... 1999: Abi-

¢ patterns of many taxa that evolved through gla- es. Tsumura & Suyama, 1998). Lineage sorting, as
cial cycles or vicariance events have been well а result of a short period for coalescence, contrib-
demonstrated based on genealogical information of шей to the low level of differentiation (Chiang,
organelle DNA (e.g.. Pinus, Latta & Mitton, 1997: 2000). Nevertheless. Manos et al. (1999) showed
Abies, Tsumura & Suyama, 1998: Cycas, Huang et that monophyly of organelle DNA haplotypes could
al., 2001; Fagus. Demesure et al., 1000: Quercus. be attained in some recently evolving species. In
Petit et al.. 1997: Alnus, King & Ferris, 1998; Kan- their study, cpDNA of. Quercus tomentella (sect.
delia. Chiang et al.. 2001: and Beta, Desplanque — Protobalanus) was proved monophyletic, while its
et al.. 2000). most related con-sectional species Q. cedrosensis.

High levels of genetic variation were usually de- as well as most other species, remained paraphy-
tected in these species, in part due to their long letic. Processes such as fluctuation in population
evolutionary history. However, the distribution of size. gene migration. and selection affect the ge-

genetic diversity varies widely between plant spe- nealogical relationships among haplotypes (Schaal.

(Тїз research has been supported by NSC and COA grants of Taiwan to T. Y. Chiang.
? Institute of Biodiversity, Cheng-Kung Unive rsity. Tainan. Taiwan 701.

' De ‘ana nt of Biology, С һе и Кг University, Tainan, Taiwan 701.

! Division of Botany, Institute of Endemic Species Researc th, Nantou, Taiwan.
> Corresponding author, email address: tychiang@ mail ne pris hiis

ANN. Missourt Bor. GARD. 91: 207-222. 2004.

208

Annals of the
Missouri Botanical Garden

2000). In general, coalescence of neutral alleles
(such as noncoding spacers) of maternally inherited
organelle DNAs (Rebound & Zeyl, 1994) is regu-
lated by duration of isolation, population number
and size, and other evolutionary agents, such as
migration (cf. Hoelzer et al., 1°

In contrast to the research frequently carried out

e

in species of continents or oceanic islands (e.g..
Hawaii, Stuessy & Ono, 1998), less attention has
been paid to plants of continental islands (e.g., Abi-

Tsumura & Suyama, 1998; Cunninghamia, Lu
et al., 2001), which had been a part of the adjacent
mainland before geographical separation. Com-
pared to taxa of European and American conti-
nents, the distribution of most plants on a conti-
nental island such as Taiwan is constrained due to
its small area and rugged landscape. In addition,
in the last decades, many species of lowland areas
have been under threat because of habitat destruc-
ion, activities. The
effect of random genetic drift could be a more im-
portant factor in those island plants with reduced
population sizes. Then, low levels of genetic vari-
ation within species would be expected.

a result of human economic

To understand phylogeographic patterns and the
gene genealogy of species of continental islands,
oaks provide ideal material. A great number of data
are available for species of continents of Europe
and North America (Whittemore & Schaal, 1991:
Manos et al., 1999), and the fagaceous plants share
similar breeding systems and demography. In Tai-
wan, Lithocarpus species are highly diverged, with
14 species recognized (Yang et al., 1997). Like
many endemic species that survived glacial cycles
on the island, a large number of relictual Lithocar-
pus species, such as L. castanopsisifolius (Hayata)
Hayata and L. konishii (Hayata) Hayata, are spo-
radically distributed with limited population sizes,
partly due to biogeographic history and recent hu-
man disturbance (Lin, 1966). The taxonomy of Tai-
wan’s oaks has been well documented (Liao, 1996:
Huang et al., 1999). Some species complexes have
long puzzled taxonomists, including Lithocarpus
Jormosanus (Hayata) Hayata and L. dodonaeifolius
(Hayata) Hayata. Kudó (1931: 387) recognized the
latter within L. formosanus (as Synaedrys |: Litho-
carpus] formosana fo. dododaeifolia), and Li (1953)
also suggested a conspecific relationship. In con-

trast, recent. taxonomic treatments (Liao, 1996;
Yang et al., 1997) recognized two separate species.

Trees of 4-9 m in height from both taxa in Lith-
ocarpus share entire leaf margins and a rounded
leaf apex. The oblanceolate leaf shape of Lithocar-
pus dodonaeifolius is distinct from the elliptic leaf
shape of L. formosanus. In addition, shorter petioles

(4—8 mm), longer infructescence (3—5 cm), and taw-
ny tomentose cupule bracts characterize L. dodon-
aeifolius, while longer petioles (10—13 mm), shorter
infructescence (ca. 3 cm), and gray tomentose cu-
pule bracts occur in L. formosanus. Lithocarpus for-
mosanus and L. dodonaeifolius are allopatrically
distributed in southern Taiwan about 30 km apart.
A single extant population of L. formosanus, con-
sisting of no more than 100 plants, remains in the
wild, although several scattered populations were
previously recorded (cf. Lu, 1996). This population
is distributed along the Nanjen Stream in the
Kengting National Park. Two subpopulations of L.
formosanus occurring along ridges about 400 m alt.
are separated by the Nanjen stream. In contrast,
three populations of L. dodonaeifolius are distrib-
uted along the Central Mountain Range of the Tai-
wanese island: Mt. Weiliaoshan (with about 100 in-
dividuals, 1200 m alt.), Chingshuiying (with
about 200 individuals, ca. 1500 m alt.), and Dazen
(with 9 individuals, ca. 600 m alt.). These three
populations of L. dodonaeifolius are isolated by dis-
tances between 20 km and 60 km. Ecologically,
both species usually grow on wind-facing slopes,
mixing with other species of Fagaceae and Laura-
ceae in tropical or subtropical forests.

Organelle DNA is maternally inherited in oaks
(Dumolin et al.,

ca.

1995) and can only migrate across
populations via seed dispersal. An "isolation by
distance" model would be expected in oaks, whose
seed dispersal is constrained by the migratory ca-
pability of the seed carriers. In addition, as a result
of stochastic drift, coalescence of cpDNA alleles in
populations with small size can be possibly
reached. Nevertheless, both ongoing gene flow and
historical migratory events have influenced the
amount of genetic variation between and within
species/populations. In this study, we looked into
the stage of lineage sorting of the chloroplast DNA
locus at a noncoding spacer located between atpB
and rbcL genes between and within the two endem-
ic Lithocarpus species. One population is limited in
both population size and number, while the other

possesses relatively healthy population structure.

Based on genealogical relationships among alleles
of the cpDNA locus, the phylogeographic pattern
of the Taiwan's Lithocarpus species was reconstruct-

In order to determine the level of ongoing gene
flow between populations, RAPD fingerprints,
which are mostly amplified from the nuclear ge-
nome (Hawkins & Harris, 1998), were utilized to
assess the extent of migration. In the study, several
objectives are pursued: (1) the partitioning pattern
of cpDNA variation within and between species; (2)

Volume 91, Number 1
04

Chian 209

g et al.
Lineage Sorting and Phylogeography

the possible migratory mode of Taiwan’s oaks over
the geological history; (3) the coalescence process
alleles within species and a emite

ү

MATERIALS AND METHODS
POPULATION SAMPLES
A single population of Lithocarpus formosanus

and three Meam of L. ananas ови were sur-
. these populations

veyed (Table 1). Geog
are 20-95 km ae. Except fas the complete sam-
pling in the Dazen population of nine, about 10%
of wild individuals were sampled randomly (Table
1). Both species of Lithocarpus grow on the wind-
facing slopes. Young and healthy leaves were col-
lected in the field, rinsed with tap water and dried
in silica gel. Voucher specimens were deposited at
NCKU at Cheng-Kung University. All samples were
stored at = 70°С until they were processed.

DNA EXTRACTION, AND NUCLEOTIDE
SEQUENCING

PCR,

Genomic DNA was extracted from Lithocarpus
leaf tissues following the CTAB procedure (Murray
& Thompson. 1980). PCR amplification was carried
out in a 100 pl. reaction using 10 ng of template
DNA, 10 pl of 10X reaction buffer, 10 pl MgCl,
(25 mM). 10 pl dNTP mix (8 mM), 10 pmole of each
primer, LO pl of 10% NP-40, and 2 U of Tag poly-
merase (Promega, Madison, Wisconsin, U.S.A.). The
reaction was programmed on an MJ Thermal Cycler
(РТС 100) as one cycle of denaturation at 95°C for
ЗО cycles of 45 sec denaturation at 92°C, |
30 sec.
followed by 10 min. extension at

4 min.,
min. 15 sec. annealing at 52°C, and 1 min.
extension at 72°C,
72°C. Template DNA was denatured for 4 min. (first
cycle), and cooled on ice immediately. A pair of uni-
versal primers for cpDNA atpB-rbcL spacer (Chiang
et al., 1998), dNTP. and Taq polymerase were added
to the above ice-cold mix. Reaction was restarted at
the first annealing at 52°С.

PCR products were purified by electrophoresis
in 1.0% agarose gel using 1 X TAE buffer. The gel
was stained with ethidium bromide, and the desired
DNA band was cut and eluted using agarose gel
purification (QIAGEN). Eluted PCR products were
directly sequenced in both directions by standard
methods of the Tag dye deoxy terminator cycle se-
quencing kit (Perkin Elmer) on an Applied Biosys-
tems Model 377A automated sequencer (Applied

Biosystems).

SEQUENCE ALIGNMENTS AND PHYLOGENETIC
ANALYSES

Nucleotide sequences of atpB-rbel, nonc oding

spacer of cp were registered with EMBL

dle 1). Nucleotide sequences were aligned with ia
program Genetics Computer Group (GCG) Wiscon-
sin Package (Version 10.0, Madison. Wisconsin)
and later adjusted visually. Neighbor-joining (NJ)
analysis, calculating Kimura’s (1980) two-parame-
ter distance and excluding the gaps, was performed
using software MEGA (Kumar et al., 1993). Confi-
dence of each reconstructed clade was tested by
bootstrapping (Felsenstein, 1985) with 1000 repli-
cates using unweighted characters. The nodes with
bootstrap values greater than 0.70. as a rule of
thumb, are significantly supported with = 95%

probability (Hillis & Bull, 1993).

mutations between haplotypes in pairwise compar-

The number of

isons, calculated using “number of differences” im-
plemented in MEGA (Kumar et al., 1993), was used
to construct a minimum spanning network with the
aid of the MINSPNET (Excoffier & Smouse. 1994)
in an hierarchical manner (Chiang & Schaal, 1999).
After linking the related haplotypes into a clade,
closely related clades were linked further to form
higher level groups and thereby a network.

RAPD FINGERPRINT ANALYSIS

We used the polymerase chain reaction (PCR)
with arbitrary primers for obtaining RAPDs follow-
ing Williams et al. (1990). We used 5 ng of DNA
template, 0.3 uM primer (Operon Technologies, Al-
Мер үе l unit of Taq polymerase (Pro-
mega), wh of PCR buffer, 2.5 mM MgCl,, and
100 1 of each dNTP for each 25 pl. PCR reac-
поп. respectiv

PCR amplifica ation took place in a PTC-100 ther-
mal cycler (MJ Research Inc.) programmed for an
initial 3 min. denaturation at 94°C, 35 cycles of 20
sec. at 94°C, 30 sec. at 36°C, at 72°C,
followed by a 10-min. final extension at 72°С. Forty
10-base

ameda.

and 90 sec.

primers were screened
from the Operon (Alameda, California) K and №
series (OPK-01—OPK-20; OPN-01 —OPN-20).
RAPD products were electrophoresed on 2% Nu-

oligonucleotide

sieve 3:1 agarose gels, stained by ethidium bro-
mide, and photographed with Polaroid type 667
film

A RAPD data matrix based on the presence and
absence of loci was prepared by the aid of AMOVA-
PREP (version 1.01; Miller, 1998). We used AMO-
VA version 1.55 1992) to deduce

the significance of geographical divisions both be-

(Excoffier et al.,

tween populations and between regions. The statis-

Missouri Botanical Garden

Annals of the

210

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әрцоәүәпи jo 12quinu әзрләле ay] = q ‘saouelayip әәиәпрәѕ Jo Jequinu әделәлв əy} = H ‘pelRorpul әле (шу) sjuo4a uorneurquioo21 umunuiw pue *(fiff) хиѕләлір әрцоәрәпи
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Volume 91, Number 1
2004

Chiang et al. 211

g
Lineage Sorting and Phylogeography

tics of molecular variants PCT (among regions). PST
(among populations). and PSC (among populations
within a region) were estimated (cf. Chiang et al.,
2001). of these F-statistic
logues was evaluated by 1000. random. permuta-

The significance ana-

tions. The UPGMA dendrogram of populations was
drawn based on pairwise dissimilarities using soft-

ware TFPGA (version 1.3: Miller, 1997).

POPULATION GENETIC ANALYSIS OF THE cpDNA
AND mtDNA SEQUENCE VARIATION

Levels of inter- and intra-population genetic di-
versity were quantified by indices of haplotype di-
versity (А) (Nei & Tajima, 1983) and pairwise es-
timates of nucleotide divergence (Dij) (Jukes &
1964) using DnaSP (Version 3.0. Rozas &
Rozas. 1999). Patterns of geographical subdivision

Cantor.

and gene flow were also estimated hierarchically
aid of DnaSP.

were

Recombination and gene
DnasP.

Gene flow within and among regions (populations)

with the

conversion events detected using

was approximated as Nm, the number of female
migrants per generation between populations. It
was estimated using the expression FST = 1/(1 +
2 Nm). where N is the female elective population
size and m is the female migration rate (Slatkin.
1993)

The pattern of "isolation by distance” was as-
sessed in both cpDNA and RAPD data by plotting
pairwise genetic distance (for RAPD) or log (Nm)
values (for cpDNA) against log (geographical dis-
Slatkin, 1993: 1998:
Stauffer et al., 1999). The significance of the as-
sociation between Nm and geographical distance

tance) (cf. Forcioli et al.

was determined by a regression F test using the
SPSS program (Norusis, 1994).

RESULTS
HAPLOTYPES. NUCLEOTIDE DIVERSITY. AND CpDNA

PHYLOGENY OF LITHOCARPUS FORMOSANUS AND V
DODON

In this study, the atpB-rbcL noncoding spacer of

cpDNA in Lithocarpus formosanus and L. dodon-
aeifolius were PCR amplified and sequenced.
Length of the atpB-rbcL spacer of cpDNA varied
from 730 bp (isolate doda36) to 935 bp (isolate
for4005). A total of 996 bp were aligned (alignment
available from authors on request), of which 201
sites (20.2%) excluding the sites with alignment
gaps were polymorphic, This noncoding spacer was
A+T rich (68.8%).
Nineteen haplotypes (h = 1.0) and 39 haplotypes
(h = 1.0) of the cpDNA noncoding spacer were

All sequences were unique.

Jorl1501 (L. formosanus)

determined in L. formosanus and L. dodonaeifolius.
respectively, according to the DnaSP analyses. Nu-
cleotide diversity (Jukes & Cantor, 1964) of
0.08074 + 0.01149 and 0.06026 + 0.00702 was
estimated in the above species, respectively. In the

largest population (Chingshuiying) of L. dodonaei-

folius, nucleotide diversity as measured by pairwise

estimates (Dij = 0.07039 + 0.00545) of the cp-
DNA was higher than that of those smaller popu-
lations (Dij = 0.04560 + 0.02224 for Dazen and
Dij = 0.04554 + 0.01690 for Weiliaoshan) (Table
П)

A neighbor-joining (NJ) tree was reconstructed
based on the genetic distance among aligned. se-
quences of the cpDNA. Four groups (A-D) were
identified and supported by bootstrap significantly
(Fig. 1). Clades B and € were grouped further, al-
though not significantly (bootstrap value = 0.52).
The monophyly of the cpDNA noncoding spacer in
dodonaetfolius was not
Nevertheless.
D consisted of individuals of L. dodonaetfolius ex-

either L. formosanus or L.
suggested by the NJ analysis. clade
clusively (Table 1). Within clade А. most sequences
of L. formosanus and L. dodonaeifolius were mixed.
except for a subcluster A^, which comprised se-
quences of the latter species only. Within the clade
B. an unusually long branch leading to ther
(L. formosanus) was identified, which differed by 49

its closest sequence of
Fig. 2).

mutational changes from

—

GENETIC DIFFERENTIATION BETWEEN LITHOCARPUS
FORMOSANUS AND L. DODONAEIFOLIUS

A minimum spanning network was constructed
based on mutational changes between sequences
(Fig. 2).
in both species agrees with the conventional cla-

Paraphyly of the cpDNA noncoding spacer

distic analysis. Two major line Fr with 98 muta-

tional changes were determined. and .
Within clade A, several ancestral м наат

| the network as interior nodes were identified:

T
isolates for203 representing Lithocarpus formosan-
us, and doda20, dodal715, dodb008, dodb009,

dodb004. for L. dodonaeifolius, indicating shared
ancestral. polymorphisms and nearly equal age of
the two species. Clade B is linked to doda20 (L.
dodonaeifolius) via for3903 (L. formosanus). Within
the second clade A”, clade B is linked to clade С

—

with 25 mutational changes, and clade D is linked
to clade C with 20 mutational changes.

Low genetic differentiation of the cpDNA locus
was detected between Lithocarpus formosanus and

An Nm of 43.75 and an FST of

Pairwise comparisons be-

L. dodonaeifolius.
0.00575 were deduced.

212 Annals of the
Missouri Botanical Garden

Lithocarpus
9: Wanlider
L. formosanus (for)

B: Chingshuiying

L. dodonaeifolius (doda)
A: Dazan

L. dodonaeifolius (dodb)
Ф: Weiliaoshan

L. dodonaeifolius (dodc)

BB doda20
- 6 for1023

pw dodb007
— @ for204

dodc003

@ dodc026

@ dodc007

O for1502

Ш doda36

0.020

B

|

Figure Neighbor-joining (NJ) tree of cpDNA of Lithocarpus formosanus and L. dodonaeifolius. Numbers in bold
at nodes 1 5 'ate bootstrap values. Four clades (A-D) and subtype A* are indicated.

213

Chiang et al.

Volume 91, Number 1

2004

Lineage Sorting and Phylogeography

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214 Annals of the
Missouri Botanical Garden

Table 2. Pairwise Vm (above the diagonal) and Ет (below 95 diagonal) н populations deduced from chlo-
roplast DNA sequences. For symbols for populations see Table Nm refers to the number of female migrants per
generation between populations. Ет = 1/1 +2Nm), where N = nal effective 1 size, m = female migrant
rate,

L. formosanus dodonaeifolius
for doda dodb dode
L. formosanus 43.74 126.89 3.14

от
L. dodonaeifolius 0.00575

doda 0.00197 1.49 1.22

dodb 0.07365 0.1439 4.65

dode 0.09638 0.1390 0.05679
tween L. formosanus with each population of L. do- the lineage A” between L. formosanus and popula-

donaeifolius also indicated high Nm values, ranging tions of L. dodonaeifolius was obtained, with a
from 2.34 to 126.89, and low FST, ranging from range between 0.06 and 2.06. Within L. dodonaei-
0.00197 to 0.09638 (Table 2). Between populations ius, clade A was not differentiated between pop-
of L. dodonaeifolius, the deduced Nm ranged from ulations according to the high deduced Nm, with a
1.22 to 4.65 and the deduced Fst ranged from range of 13.64 to 1015.96, while significant differ-
0.05679 to 0.1439. Subpopulations of L. formosan- entiation between populations was detected in the
us, which are separated by a stream, were not dif- clade A” based on the low deduced Nm (0.00—
ferentiated based on a 155 value of deduced Nm 0.42). In addition, the nucleotide diversity is higher
(40.50) and low Fsr (0.01250). as measured by pairwise estimates in the A' clade

When lineages A and rt were considered sep- (Dij = 0.04549 + 0.02237) than in the A clade
arately, within L. formosanus, both lineages were (Dij = 0.01637 + 0.01335).

differentiated significantly, with an Nm of 0.11 and Based on DnaSP analysis of sequences of both
an Fst of 0.6937 (Table 3). Low differentiation be- species as a whole, 18 possible minimum recom-
tween L. formosanus and each population of L. do- bination events were detected. Four and 15 mini-
donaeifolius was suggested based on the high de- mum recombination events occurred in L. formo-
duced Nm of the clade A (with a range of 6.83- sanus and L. dodonaeifolius, respectively. In

57.29). In contrast, the much lower deduced Nm of contrast to short DNA fragments involved in the

Table 3. Pairwise Nm (above diagonal) and Fst (below diagonal) between species and populations with lineages A
and A’ considered se d ly. Nm refers to the number of female migrants per generation between populations. FST

I(1+2Nm), where N = female effective population size, m = female migrant rate.
L. formosanus L. dodonaeifolius
for doda dodb dode

lineage A lineage & lineage A lineage A” lineage A lineage A lineage & lineage A’

L. formosanus
i A

lineage / 0.11 12.21 0.11 0.83 2.24 57.29 0.04
or

lineage A” 0.0937 0.07 2.00 0.16 0.06 0.08 0.14
L. dodonaeifolius

lineage A 0.0059 0.7755 0.07 38.85 1.00 13.64 0.01
doda

lineage A“ 0.7041 0.1081 0.7894 0.13 0.05 0.07 0.42

lineage A 0.0380 0.6129 0.0064 0.6549 2.30 1015.96 0.06
dodb

Lineage A' 0.1003 0.8193 0.2000 0.8453 0.0981 1.00 0.00

Lineage A 0.0044. 0.7464 0.0180 0.7728 0.0003 0.2000 0.02
dode

Lineage A’ 0.8766 0.6351 0.9486 0.3716 0.7992 1.000 0.9126

Volume 91, Number 1
2004

Chiang et al.
Lineage Sorting and Phylogeography

genetic recombination in I. dodonaeifolius, two
large DNA fragments, i.e., fragments of (261. 503)

and (831,

based on DnaSP analyses (Table 1).

950). were identified in L. formosanus

RAPD FINGERPRINTS AND GENE FLOW

A UPGMA dendrogram was constructed. based
on the deduced genetic distance among individuals
(Fig. 3). All

айа) together, as were those of L. dodonaeifol-

individuals of L. formosanus were
ius. Individuals of the Dazen population as well as
the Weiliaoshan population were clustered together.
both of which were nested within the group of the
The UPGMA

gram (Fig. 4) based on the TFPGA analysis. which

Chingshuiying population. dendro-
recognized each population (instead of individual)
as a unit, suggested significant differentiation. with
about 54.8% dissimilarity, between L. formosanus
and L. dodonaeifolius. In addition, within L. dodon-
aeifolius populations from Weiliaoshan and Dazen
shared highest similarity (about 85%). Based on the
deduced Nm (1.06) and Fsr (0.19149), estimating
the gene flow, the subpopulations of L. formosanus
were barely differentiated.

DISCUSSION

GENETIC VARIABILITY OF THE NONCODING SPACER
BETWEEN atpB AND rbcL GENES OF cpDNA IN
TAIWANESE OAKS

and J.

seemed to possess higher levels of cpDNA haplo-

Lithocarpus formosanus dodonaeifolius
type diversity (19 and 39 haplotypes, respectively:
Table 1) than other plants, e.g.. 13 cpDNA haplo-
types in Beta vulgaris subsp. maritima (Desplanque
et al.. 2000). 11 haplotypes in Argania (El Mou-
sadik & Petit, 1996),
(Dumolin-Lapègue et al.,

ı Alnus (King & Ferris, 1998). The nucleotide di-
versity (Dij = 0.06026 and Dij = 0.08074) of these
two Taiwanese oaks was also high, compared to that
of California pines (Dij = 0.003 + 0.002) (Hong
1993).

High level of genetic diversity in the. Fagaceae
(cf. Petit et al..
1997) is probably associated with their long evo-

23 haplotypes in white oaks
1997). and 13 haplotypes

et al.,
1997; Dumolin-Lapegue et al..

lutionary history, which allows genetic variation to
accumulate within lineages (cf. Chiang & Schaal.
1999), Nevertheless, the higher haplotype diversity
of epDNA of Lithocarpus from Taiwan may be sim-
ply derived from. different molecular techniques
employed. Nucleotide sequencing usually detects a
higher level of genetic variation than do the RFLP
and PCR-RELP techniques. In our analysis, ac-

cording to the deduced restriction site map. only
four chlorotypes (cpDNA polymorphisms) for 58 in-
Within

smaller populations of L. dodonaetfolius from Wei-

dividual haplotypes could be identified.

liaoshan and Dazen, the number of major clades
was even lower (with only two), while high levels
1) and nucleotide di-
0.045—0.046) were assessed based
on the sequence variation. As stated by Desplanque
et al. (2000),
sity in natural plants should have existed (cf

McCauley, 1994; El Mousadik & Petit, 1996: Ras-
pe, 1998). The detection of the existing variation
surely depends not only on the conservative nature

of haplotype diversity (A =

versity (Dy =

a substantial within-population diver-

of the molecular marker itself, but also the sensi-

tivity of the tools employed. In this study, the so-
called “higher” level of genetic variation of L. for-
mosanus and L. dodonaeifolius turned out much
lower than that of other species, when nucleotide
sequences were transferred to RFLP data (data not
shown). Such low level of chlorotype diversity, as
expected, may be ascribed to their smaller popu-

ation number and size.

Interestingly, Lithocarpus formosanus possessed
a much higher level of nucleotide diversity than did
L. dodonaeifolius, despite fewer chlorotypes (three
types) existing in the former species (vs. four types
for L. dodonaeifolius). In general, populations with
larger sizes maintained higher genetic variation
compared to smaller ones, such as Chingshuiying
(Dij = 0.07039) versus Dazen (Dij = 0.04560) and
Weiliaoshan (Dij = 0.04554). According to the lon-
gest branch of the for1502 (P. — 0.05) in the neigh-
bor-joining tree (Fig. 1), the unusually high nucle-

otide diversity in I formosanus was probably
ascribed to the most diverged sequence. When the

sequence of for1502 was removed from the calcu-

ation, a low level of nucleotide diversity (у =
0.07369 + 0.01161) was obtained. This deviation
from a molecular clock (P < 0.01) can hardly be
attributable to natural selection, whose effect is
usually not intense on a noncoding spacer (Graur
& Li. 2000).

dom genetic recombination within the chloroplast

Vecording to the DnaSP analysis, ran-

DNA marker may have resulted in the long branch
Huang et al.. 2001).

As a noncoding region, the afpB-rbcL spacer has
With nearly

extent would

of L. formosanus (cf.

relatively low functional. constraints.

neutral evolution. mutations to some
have been retained within each lineage. However,
extremely low substitution rates in the atpB-rbcl.
spacer have been detected in other plants (Manen
& Natali, 1995: Chiang & Schaal, 2000a, b). High
levels of genetic variation of the cpDNA of Litho-
in Taiwan may be ascribed to fre-

carpus part

216

Annals of the
Missouri Botanical Garden

Lithocarpus
©: Wanlider
L. formosanus (for)
B: Chingshuiying
L. dodonaeifolius (doda)
А: Dazan
L. dodonaeifolius (dodb)
Ф: Weiliaoshan

—

L. dodonaeifolius (dodc) ШШ

| 4 hb hb A A A 99 A 9 9 AA LD hh ha

A dodb0037 |

A dodb002
à dodb004
à dodb005

100

ppp

) for202

—

snijo/fiopuopop /

SNUDSOULAOL "T

Figure 3. UPGMA tree of individuals of Lithocarpus formosanus and L. dodonaeifolius based on RAPD data.

Numbers at nodes indicate bootstrap values.

Volume 91, Number 1
2004

Chiang e
Lineage Sete and Phylogeography

| | | | |
| Т
0.600 0.450 0.300 0.150 0.000
Weiliaoshan
Dazen Lithocarpus dodonaeifolius
Chingshuiying
Wanlider — Lithocarpus formosanus

Figure 4. UP(

„ formosanus at Wanlider; doda: L. dodonaeifolius at €

quent intramolecular recombination, a process well
documented in plant organelle DNAs (e.g.. Stern &

almer, 1984; Yesodi et al., 1997; Senda et al.,
1998; Huang et al., 2001). Large DNA fragments
involved in the intramolecular recombination of the
cpDNA may have contributed to the longer branch
leading to the forl 502. Indel events were respon-
sible for high polymorphisms of cpDNA as well. In
contrast to random genetic recombination, indel
events occurring in bp positions between 311 te

608 for the atpB-rbcL noncoding spacer appeared
nonrandom.

PHYLOGEOGRAPHY OF LITHOCARPUS FORMOSANUS=L.
DODONAEIFOLIUS AND GENE GENEAOLOGY OF cpDNA

RAPD fingerprints revealed significant differen-
tiation between Lithocarpus formosanus and L. do-
donaeifolius based on the UPGMA dendrogram and
deduced Fst. Genetic distance between popula-
tions is strongly associated with geographical dis-
tance (P < 0.05, Fig. 5A), which is consistent with
1993).

Interestingly, according to the differentiation be-

a model of isolation by distance (Slatkin,
tween subpopulations of L. formosanus on the
UPGMA dendrogram (Fig. 3), a ravine of narrower
than 1 km in width (i.e., Nanjen stream) may be-
come a natural barrier for pollen dispersal. al-
though it is not significant.

In contrast to the significant genetic differentia-
tion between species and populations indicated by

RAPD fingerprinting, which represents the level of

ongoing gene flow between populations, the cpDNA
noncoding spacer within species and populations
was non-monophyletic. The most common chloro-
type A (68.9%) was predominant over other alleles
(8.6% for В, 6.9% for С, and 15.6% for D) and was
widespread in all populations. In contrast, chloro-
type D was exclusive to Lithocarpus dodonaeifolius,
while chlorotypes B and С were distributed in £.
formosanus and the Chingshuiying population of L.

;MA tree of populations of Lithoc eds formosanus and L. о based on RAPD a for:
hingshuiyin L. do-
als at Weiliaoshan. The level of dissimilarity between wi yi is ese

g: dodb: "e onaeifolius at Dazen; dode:
ed

dodonaeifolius. The biased distribution of alleles in
populations plus low differentiation between spe-
cies suggested lineage sorting of the cpDNA locus
n both Lithocarpus species (cf. Hoelzer et al.,

1998: Young, 1998). Lineage sorting results from a
process of differentiated births and deaths, when
ancestral polymorphisms are passed down to de-
scendent lineages (populations) (cf. Futyuma. 1998;
Chiang, 2000). It usually blurs the inference of or-
ganismal phylogeny. In this study, monophyly of the
chlorotype D at species level, 1.e., within £. dodon-
aeifolius, and paraphyly of other chlorotypes indi-
cated that these chlorotypes are at different lineage
sorting periods.

The extent of lineage sorting is usually deter-
mined by the genetic heterogeneity within popula-
tions and the migratory mode, which in turn is as-
sociated with the ongoing gene flow and natural
hybridization as well as geological history that the
species evolved through. Recurrent introgression 18
typically invoked to explain such sorting (cf. Manos
et al.,
ues between species and populations deduced from

1999). However, unexpectedly high Nm val-

the nucleotide sequences of the cpDNA locus of
Lithocarpus in Taiwan and the low correlation be-
tween Nm (up to 126.89) and the geographic dis-
0.05.

mode may

tance (P > Fig. 5B) indicates that the migra-

tory have deviated from the
stepping-stone model, Wright’s island model, or an
isolation-by-distance model (cf. Hamrick & Nason,
1996).

Evidently, given limited pollen dispersal among
populations (indicated by our RAPD results), the
migration of Lithocarpus fruits or nuts across a geo-
graphic range of 20-95 km in modern habitats is
even more improbable due to the discontinuity of
vegetation and the constraint of migratory capabil-
ities of any fruits- or nuts-carrying animals. Al-
though some low levels of incidental seed dispersal
among populations cannot be simply ruled out, un-

218 Annals of the
Missouri Botanical Garden

A)
0.25
R°=0.6159 И
= +
ENUF
yo)
= 0.1 р
©
= 0.05 F

i)

B)

ў
2
,| R-0001 :
m,
Е 1.5 F
Z
—
Ыы)
G If
a „
0.5 +
*
() П | | Ф 1
0 0.5 1 | А io
log(km)
Figure 5. — A. Scatterplot of genetic distance and logarithmic scales of ge ppr distance — populations of
L. dodonaeifolius haved on RAPD data. Regression statistics: А? = 0.6159, P >. —B. Scatterplot of logarithmic

scales of Nm and geographic distance among populations of Lithoc arpus piii and L. 1 ifolius base x on on
chloroplast DNA variation. Regression statistics: R? = 0.0091, P > 0.05. N = female effective population size, m =
female migrant rate.

usually high Nm values are likely to represent his- tween populations suggested a migrant-pool model,
torical migration events instead of the current gene а migratory pattern with colonists recruited from a
flow. Low genetic differentiation due to shared and random sample of all the other populations (Wade
heterogeneous composition of organelle DNAs with- & McCauley, 1990). Usually this model is associ-
in each population and the high deduced Nm be- ated with glaciation or vicariance events, which ac-

Volume 91, Number 1
2004

Chiang et al.
Lineage Sorting and Phylogeography

cording, to fossil evidence may disturb the vegeta-
tion dramatically at a large geographic scale.
Like many angiosperm species (e.g.. Fagaceae,
1995, Petit et al., 1997, Dumolin-
1997: beeches, Koike et al., 1908:
and beets, Desplanque et al., 2000) and. gymno-

Ferris et al.,

apegue et al.,

sperms, such as Cunninghamia (Lu et al.. 2001) as
well as Pinus (Strauss et al., 1993), oaks survived
cf. Bennett, 1990;

According to geological record,

Huang et al.,

—

glacial cycles
2001).

late Pleistocene.

since the
Taiwan was the southeastern edge
of the Asian continent before the formation of Tai-
wan Strait about 100,000 BP (Lin. 1906; Tsukada.
1966: Kizaki & Oshiro, 1977). This continental is-
land was linked to the mainland via a land bridge
and was not completely isolated until the last gla-
3.000 to 20,000 BP (Lin. 1900).

Geological evidence indicates that ice ages have

cial retreat ca. lé

occurred at regular intervals of approximately
100,000 years followed by warm periods of about
20,000 years (Milankovitch cycles) (ef. Bennett.
1990; King & Ferris, 1998). During the glacial
maximum many oaks and conifers previously dom-
inant in the northern part of eastern Аға were
forced to migrate into refugia in southern China and

1999),

low elevations (cf.

which were mostly
Tsukada, 1960).

During the subsequent deglaciation, elevated glob-

Taiwan (Chiang et al.,
distributed

al temperatures forced the lowland plants to mi-
grate to high elevations or local peaks. Pollen re-
cords reveal the migration routes of many relictual
and endemic species, which constitute a large por-
tion of Taiwan’s flora (Shaw, 1997). The current geo-
graphical distribution of Lithocarpus dodonaeifolius
and L. formosanus is possibly a result of such a
migration history.

According to the shared cpDNA alleles of the
atpB-rbel, noncoding spacer, the speciation of Lith-
ocarpus dodonaeifolius and L. formosanus may be
recent. Like other fagaceous plants, migration via
1997) of

the ancestral populations of the Taiwan oaks be-

long-range seed dispersal (cf. Petit et al.,

came possible due to the dramatic change of veg-
etation (cf. Chiang & Hong, 1999) during deglaci-
ation.
plants that survived after species extinction. Seeds

Many novel niches were then available for

from different resource populations may have mi-
grated into the refugia and settled subsequently.
Such migration may have increased the heteroge-
neity of cpDNA composition within populations.
Extinction and re-colonization regulated by geo-
logical events, however, were thought to enhance
genetic differentiation among populations (cf.
Wright,

from the colonization by a small number of surviv-

1977) owing to founder events resulting

Wade and

McCauley

(1990) further suggested that the results of extinc-

ing individuals. Recently,

tion/re-colonization on genetic differentiation
among populations depend on the number of found-
ers as well as the level of heterogeneity of genetic
composition within populations according to coa-
lescence theory. When the colonist size is small and
the genetic heterogeneity is low, genetic differen-
tiation among populations will be reached fast via

stochastic processes alone.

Despite the relatively small population. size in
both Lithocarpus species, no coalescence has been
achieved within populations. To counter the genetic
diversity loss within small populations due to ge-
netic drift, it is likely that the genetic composition
of ancestral populations, even species, prior to de-
glaciation as well as succeeding colonizing popu-
lations was highly heterogeneous. The four chloro-

types noted for these two Lithocarpus species in

Taiwan may have existed long before the speciation
event. In addition, recurrent genetic recombination
within the chloroplast intergenic spacer may have
increased the heterogeneity within species as well.
Given small population sizes, the low level of ge-
netic differentiation among Lithocarpus populations
at the cpDNA noncoding spacer region is possibly
ascribed to a short duration (since the last degla-

ciation) for coalescence.

Aneage sorting (or the attainment of monophyly)
f chlorotypes within species and populations is as-
suredly drift
(Chiang. 2000). The high frequency of the chloro-

regulated by the stochastic genetic
type A over others in both Lithocarpus species and
the high frequency of the chlorotype В in L for-
(80%) illustrate this random effect. With

a short time span for coalescence, monophyly of the

MOSANUS

cpDNA locus has not been attained within either
species. The chlorotype D may have been drifted
in L. formosanus due to its smaller population size.
Obviously, the larger population (200 individuals)
at the Chingshuiving site possessed higher genetic
variation compared to the other populations of L.

Weili-

aoshan and Dazen populations for L. dodonaeifolius

dodonaeifolius. Low genetic diversity in
is ascribed to the lack of chlorotypes B and C. De-
duced Nm values seemed to be indicative of line-
age sorting in clades A and A” (Table 3). Lower Nm
among populations derived from clade A” relative
to clade A indicates a higher level of coalescence,
e.£.. the fixation of chlorotype D in £. dodonaeifol-
ius. Drift of rare chlorotypes in smaller populations
(D in IL. formosanus as well as B and € in Weili-
aoshan and Dazen populations of L. dodonaetfolius)
thereby resulted in higher levels of genetic differ-
entiation and genetic diversity compared to the

220

Annals of the
Missouri Botanical Garden

widespread and dominant chlorotype A across pop-
ulations of both species. However, differences of
deduced Nm values between clades A and A' re-
vealed problems and limitations with the interpre-
tation of such indirect estimates of gene flow among
populations (cf. Bossart & Prowell, 1998)

In contrast to the lineage sorting of the cpDNA
locus, RAPD fingerprints attained “coalescence” at
most loci and resulted in significant genetic differ-
entiation between species. This coalescence at pop-
ulation level, however, has not been completely
reached. Interestingly, subsets of smaller popula-
tions from Weiliaoshan and Dazen for Lithocarpus
dodonaeifolius were nested within the cluster o
thingshuiying individuals, as indicated by the
UPGMA tree (Fig. 3). Coherence of smaller popu-
lations versus the division seen in RAPD sampling
within the larger population indicated such a ran-
dom coalescence process. Incongruence between
organelle DNA and RAPD fingerprints, which are
usually не from the nuclear genome (Haw-
s, 1998), may derive from the different
Ша punit between the two genomes. Ge-

kins & Har

netic recombination between homologous chromo-
somes may have played a determining role in ho-
mogenizing the genetic differences within demes
and thereby increasing the heterogeneity between
populations, while crossing-over is usually lacking
in organelle DNAs due to its haploid nature.
Accordingly, gene flow between Lithocarpus do-
donaeifolius and L. formosanus may have been
blocked since their postglacial resettlement. Adapt-
ing to habitats at different elevations as they occur,
both Lithocarpus flower with a lag interval of about
half a month. The reproductive barriers between
the two species may be complete. In contrast to
many European and American Fagaceae (Whitte-
more & Schaal, 1991; Howard et al., 1997; Manos
1999; Samuel, 1999), which hybridize nat-
urally when populations are sympatrically distrib-

et al.,

uted, no interspecific hybrids have been reported
in these Taiwanese Lithocarpus.

CONTINENT-ISLAND DISCREPANCY IN VARIATION
ALLOTMENT

At the intraspecific level, patchy structure of lo-
cal populations (e. E 1996;
‚ 1997; Dumolin-Lapègue et

Aquilegia, Strand et al.,
Fagaceae, Petit e
al., 1999) or eatin subdivision between long
isolated populations (e.g., northern and southern
populations of Liriodendron tulipifera L., Sewell et
al. 1996; Sarmathic-Baltic and Alpine—Central
European populations of Picea abies (L.) Н
Vendramin et al.,

arst.,
2000) have been documented in

many tree species of continents. Low level of or-
ganelle DNA differentiation among local popula-
tions was detected in Lithocarpus dodonaeifolius
and L. formosanus as well as other plants of con-
tinental islands, such as Cycas taitungensis Shen et
al. (Huang et al, 2001), Amorphophallus (cf.
Chiang & Peng, 1998), Michelia formosana (Ka-
nehira) Masamune (Lu et al., 2002
well as Japanese Abies (Tsumura & Suyama, 1998).

) of Taiwan as

Due to the limited area and available habitats of
the island, the population size of Taiwan's oaks is
effectively smaller than that of continental species.
Under near neutrality, a long period of lineage sort-
ing for cpDNA chlorotypes in small populations
may be likely ascribed to high levels of heteroge-
neity in genetic composition. Interestingly, greater
genetic variation has been noted in southern con-
tinental refugia (such as Italy, the Balkans, and the
Iberian Peninsula) than in northern ни
(e.g., Central Europe) (European oaks, cf. Dumolin-
Lapégue et al., 19 98; European Alnus, King
& Ferris, 1998; Faut Demesure et al., 1996; and
Japanese Abies, 1998). The
continent-island discrepancy may be associated
with the fact that Taiwan, which is straddled across
today's subtropics to tropics, is much more south

Tsumura & Suyama,

than most areas of European and American conti-
nents geographically. Taiwan may have provided
more fitting habitats for surviving plants during the
glacial maximum than mainland refugia.

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Volume 91, Number 1. pp. 1-222 of the ANNALS OF THE MISSOURI BOTANICAL GARDEN
was published on April 6. 2004.

vw.mbgpress.org

CONTENTS

A Revision of Trisetum, Peyritschia, and Sphenopholis (Poaceae: Pooideae: Aveninae) in
Mexico and Central America
-Victor I. Finot, Paul M. Peterson, Robert J. Soreng & Fernando O. Zuloaga
RÊ 4 Metastelma (Apocynaceae—Asclepiadoideae) in Southwestern North America
and Central America Sigrid Liede & Ulrich Meve

A Taxonomic Revision of the Paeonia anomala Complex (Paeoniaceae) __
Hong De-Yuan & Pan En: Yu
ир of Smelowskia and Related Genera (Brassicaceae) Based on Nuclear ITS DNA
and Chloroplast trnL Intron DNA Sequences Suzanne I. Warwick,
. —— Ihsan A. Al-Shehbaz, Connie A. Sauder, David F. Murray & Klaus Mummenhoff
Phylogenetic Relationships of Vulpia and Related Genera (Poeae, diri Based on
Analysis of ITS and trnL-F Sequences
Pedro Torrecilla, José-Angel López-Rodríguez & Pilar Cataláre
Geographical Diversification of Tribes Epilobieae, Gongylocarpeae, and Onagreae
(Onagraceae) in North America, Based on Parsimony Analysis of Endemicity and
Track Compatibility Analysis
Шапа Katinas, Jorge V. Crisci, Warren L. Wagner & Peter C. Hoch
F loral Miles: p ы (Iridaceae: Crocoideae): How Minor Shifts in Floral
Presentation Change the Pollination System
Heier Goldblatt, Ingrid Nünni, Peter Bernhardt & John С. Manning
Lineage Sorting and: Phylogeography in Lithocarpus formosanus and L. dodonaeifolius
m dence) from T.

Tzen-Yuh Chiang, Kuo-Hsing Hung, Tsai-Wen Hsu & Wen-Luan Wu

(Cover illustration. — Trisetum ligulatum Finot & Zuloaga, drawn by Vladimiro Dudás. ———

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This paper n 1

Ё AARICIsSAIICC AQ 100^ 5.
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Volume 91 Annals
Number 2 of the
2004 Missouri

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Garden

REVISIÓN TAXONÓMICA DEL Osvaldo Morrone, Silvia S. Denham? y
GÉNERO PASPALUM GRUPO Fernando О. Zuloaga?

ERIANTHA (POACEAE,

PANICOIDEAE, PANICEAE)!

RESUMEN

El grupo Eriantha de и ا‎ nde cinco especies: P ammodes, P. erianthoides, r MUN Р, guitatum
Mé

y P. pauc ifolium, que se distribuyen desde México, en América del Norte, hasta d к Bolivia, Paraguay, Argentina у
Uruguay. En el presente tratamiento se definen los caracteres morfológicos del grupo y se incluye una clave para
identificar las especies, descripciones, ilustraciones, fotografías y mapas de nie ion de las mismas. Se discuten

ogra
as relaciones de Eriantha con taxones afines de Paspalum. Finalmente, se designa un lectótipo para и erian-
thum Nees var. strictum Döll.

ABSTRACT

E is an American group of 1 with five species distributed from Mexico in North America to Brazil.

Bolivia, Paraguay. Argentina, and Urugue disi с. ammodes, P. erianthoides, P. erianthum, P. guttatum. and Р.
pauc ifolium. ириси ‘al characteristics of the group аге Ы. апа а key to identify the species, descriptions,
illustrations, photomicrographs, and distribution maps are provided. Re (иб ships of Eriantha with related taxa of
Paspalum are discussed. Finally, a lectotype was de: MS for Paspalum erianthum Nees var. strictum Doll.

Key words: America. Eriantha. Paspalum, Poaceae

Paspalum L. incluye aproximadamente 320 es- ga et al., 2003). El género fue dividido en subgé-
pecies distribuidas en regiones tropicales y subtro- neros, secciones o grupos informales por diversos

picales de América, con cerca de 20 especies en autores, principalmente sobre la base de caracteres
el Viejo Mundo (Clayton € Renvoize, 1986; Zuloa- morfológicos de la inflorescencia, espiguillas y an-

! Deseamos expresar nuestro agradecimiento a los curadores de los herbarios 5 al Sr. Vladimiro Dudás
por las excelentes ilustraciones ao acompañan esta contribución y a la Lic. Alejandra Garbini por el armado = los
трае, "arte de este estudio se llevó a cabo con fondos de la National Geographic om iety, subsidios 5334-94, #0042-
97 у #6698-00, que permitieron di trabajos de campo y del Consejo Nacional de Inve 'stigaciones Cie eer as у
Тес! nicas, CONICET, Argentina, PIP-0213

? Instituto de Botánica Darwinion, Labardé n 200, Casilla de Correo 22, San Isidro B1642HYD, Argentina. omorrone@
darwin. edu. ar.

ANN. Missouni Bor. GARD. 91: 225-246. 2004.

226

Annals of the
Missouri Botanical Garden

tecios (Nees, 1829; Doell. 1877; Chase, 1929; Pil-

E nig 1940; Clayton & Renvoize, 1986; Fil-
s & Davidse, 1994; Morrone et al., 1995,
1906, 20003 Cialdella et al., 1995; Rodriguez.

1999; Denham et al., 2002). Sin embargo no existe
un esquema natural de clasificación del género. Zu-
loaga y Morrone (en prensa) reconocen en Paspa-
lum 3 subgéneros, subg. Anachyris Chase, subg.
Ceresia (Pers.) Rchb. у subg. Paspalum, e indican
que en este ultimo subgénero atin no se encuentran
caracteres diferenciales sólidos para establecer ca-
tegorías infragénericas, por lo que se ha adoptado
el concepto de grupos establecido por Chase (1929,
inéd).

Pilger (1929) establece la sección Erianthum e
incluye a Paspalum erianthum Nees ex Trin.,
Р, sordidum Hack. (= P. am-

modes Trin.); distingue a la sección principalmente

erianthoides Lindm. y

por sus espiguillas velludas.

Swallen (1967) establece diez nuevas especies
en el grupo Eriantha: Paspalum album, P. involu-
tum, P. mollifolium, P. rigens, P. formosulum, P.
intosum, P. haughtii, P. sericatum, P. paucifolium y
P. diamantinum.

Hasta el presente no se han llevado a cabo es-
tudios del conjunto de las especies de Eriantha, y
éstas sólo han sido tratadas parcialmente en estu-
dios florísticos o regionales (Chase, 1929; Burkart,
1969; Rosengurtt et al., 1970; Sendulsky & Bur-
man, 1978, 1980; Judziewicz, 1990; Killeen, 1990;
Renvoize, 1984, 1988, 1998; Pohl & Davidse,

El objetivo del presente trabajo es el estudio de
las especies del grupo Eriantha de Paspalum, es-
tablecer los caracteres diagnósticos a nivel del gru-
po y de sus especies sobre la base de datos exo-
morfológicos. El trabajo aporta descripciones,
ilustraciones, clave para la identificación de las es-
pecies, microfotografías de antecios superiores con
microscopía electrónica de barrido, mapas de dis-
tribución y ecología de las mismas. Cabe destacar
que en la presente revisión no se ha buscado, al
agrupar taxones en el grupo Eriantha, establecer
categorías taxonómicas a nivel infragenérico.

HISTORIA

Nees (1829) divide a Paspalum en seis seccio-
nes. Bajo la sección Lanigeri trata a P. guttatum,
P. erianthum y P. sanguinolentum junto con P. ova-
dilatatum Poir.). P.
polyphyllum Nees ex Trin. > blepharophorum
Roem. & Schult. (= P. humboldtianum Fliiggé),
conjugatum Bergius y otras especies consid аА

Nees ex Trin. (= P

actualmente en Axonopus P. Beauv.

Doell (1877) agrupa a las especies de Paspalum
en cuatro secciones: Eremachyrion, Opisthion, Em-
prosthion y Cabrerae. Doell incluye en Opisthion a
P. ammodes, P. guttatum Trin., P. sanguinolentum
Trin. y Р erianthum, entre otras especies afines.

Nash (1912) al estudiar las especies de Paspa-
lum de Norte América reconoce informalmente, sin
establecer un rango determinado, a Eriantha por
incluir plantas con espiguillas pilosas en toda su
superfice y cañas simples. Nash incluye una sola
especie bajo Eriantha, P. erianthum.

Pilger (1929) divide al género Paspalum en ocho
secciones: Eupaspalum, Anachyris, Pterolepidium,
Hriunthum, Cymatochloa, Ceresia, Eriolepidium y
Moenchia. Pilger establece la sección Erianthum
sobre una parte de la sección Lanigeri de Nees
(1829) representada por P. erianthum; cabe desta-
car que del resto de especies tratadas por Nees
(1829) en la sección Lanigeri, P. obtusifolius y P.
fissifolius pertenecen actualmente a Axonopus, P.
eucomum, P. polyphyllum, y su sinónimo P. blep-
harophorum se ubican en el subgénero Ceresia, P.
ovatum en el grupo Dilatata y P. conjugatum en el
grupo Conjugata; finalmente P. ammodes, P. gut-
tatum y P. sanguinolentum (= P. erianthum) son
aquí consideradas dentro de Eriantha. Pilger (1929)
caracteriza a la sección por los racimos más o me-
nos rectos, raquis delgados, espiguillas sedosas y
velludas; incluye en la sección a P. erianthum, P.
erianthoides y P. sordidum

hase (1929) iA a Paspalum sanguino-
lentum (= P. erianthum) en el subgénero Ceresia,
aunque indica claramente que Eriantha no perte-
nece a Ceresia. Posteriormente, Chase (inéd.) trata
a Paspalum erianthum, P. rufum Nees ex Steud., P.
hassleri Hack. (= P. rufum), P. erianthoides, P. du-
rifolium Mez y P. devincenzii Parodi (= P. durifo-
lium) en el grupo Eriantha; mientras que ubica a
P. guttatum y P. ammodes en el subgénero Ceresia.

Clayton y Renvoize (1986) reconocen, siguiendo
parcialmente el criterio de Pilger (1929, 1940),
ocho secciones dentro de Paspalum; caracterizan a
Erianthum por tener espiguillas pilosas, con pelos
sedosos y citan, dentro de la sección, a P. erian-
thum.

MATERIALES Y METODOS

El estudio d fue realizado sobre la
base de especímenes provenientes de los siguientes
herbage: BM, COL, CTES, С, IBGE, ICN, K, LIL,

‚ MEXU, MO, P. R. RB, SI, SP, US y
W. Dents del material examinado de cada especie
sólo se citaron ejemplares representativos de cada
país; una lista completa de los especímenes estu-

Volume 91, Number 2
2004

Morrone et al. 227

Paspalum Grupo Eriantha

diados, ordenados alfabéticamente por coleccionis-
ta, se encuentra al final del texto (Apéndice 2).

Las fotomicrografías de antecios superiores se
realizaron de acuerdo a los procedimientos descrip-
tos por Soderstrom y Zuloaga (1989). Se empleó un
microscopio electrónico de barrido (MEB) Zeiss
940 A, perteneciente al Instituto de Botánica Dar-
winion, y se operó a 10-20 kV.

MORFOLOGÍA
FORMA BIOLÓGICA

El grupo Eriantha de Paspalum incluye especies

perennes, cespitosas, con rizomas de entrenudos
cortos o rizomatosas, con rizomas arqueados en P
paucifolium. Las cañas floríferas son erectas y sim-
ammodes, P. guttatum y P.
tener hasta 8 nudos en Р

ples, paucinodes en P.
paucifolium o pueden
erianthum. Las vainas son predominantemente ba-
sales en P. ammodes, P. erianthoides, P. guttatum
y P. paucifolium y basalcs:o: Шаш Бана a lo largo
de toda la cafia en P. erianthum; en P. ammodes,

P. erianthum y P. guttatum las vainas son senes-

centes y persistentes, fibrosas y laciniadas en la
base de las plantas; la pilosidad de las vainas varía
de glabras a densamente hirsutas o vilosas. Las lig-
ulas son membranáceas, breves, de 0.2—0.8 mm en
P. ammodes, P. erianthum y P. guttatum, de 0.5—
1.4 mm en P. paucifolium y más largas, de 1-2 mm
en P. erianthoides; en P. erianthum y P. paucifolium
no hay pseudolígula, mientras que en Р. erianthoi-
des y P. guttatum está formada por un arco de pelos
de 0.5-2 mm de largo por detrás de la lígula junto
a la unión con la lámina; la pseudolígula puede
estar presente o ausente en P. ammodes; el cuello
varía de glabro a piloso. Las láminas son lineares
en H ammodes y P. guttatum, lineares a linear-
lanceoladas en B paucifolium y linear-lanceoladas
a lanceoladas en H erianthum, mientras que P.
erianthoides presenta láminas filiformes y macizas;
P. erianthum y P. guttatum poseen láminas planas
a involutas, mientras que en E ammodes son planas
a plegadas y planas en P. paucifolium; las bases de
las láminas son atenuadas o redondeadas a sub-
cordadas, en P. erianthum pueden variar de redon-
deadas a atenuadas formando un pseudopecíolo rí-

gido; el ápice de las láminas va de agudo a
1 Dade: la pilosidad de las láminas es variable
hasta en una misma especie, desde glabras a pi-

losas en ambas Caras.

INFLORESCENCIAS

Los pedúnculos exertos llevan inflorescencias

terminales con racimos adpresos, en Paspalum

erianthoides, a divergentes y ascendentes en las
restantes especies. El número de racimos varía de
(1)2 a 11 por inflorescencia, siendo alternos a su-
bopuestos en P. erianthum, subconjugados en P
guttatum o alternos en las restantes especies; e

raquis de los racimos es de 1-12 cm de largo y
0.4-1.8 mm de ancho, triquetro en Р ammodes y
P. ertanthoides, o con una de las caras aplanada en
P. erianthum, P. paucifolium y aplanado y corta-
mente alado en P. guttatum; el raquis de los raci-
mos puede terminar en una espiguilla desarrollada
u ocasionalmente puede terminar en una prolon-
gación estéril, con espiguillas parcialmente desa-
rrolladas en P. guttatum. Las espiguillas son soli-
tarias en P. guttatum y P. ammodes y en pares en
P. ertanthoides, P. paucifolium y P. ertanthum, don-
de es frecuente que la espiguilla inferior no se de-
sarrolle por completo y persista como un rudimento
en la base de la espiguilla superior.

ESPIGUILLAS

Las espiguillas son elipsoides a largamente elip-
soides, de 2.4-5(-5.8) mm de largo y 1-2 mm de
ancho, plano-convexas, pilosas, con pelos sedosos,
blanquecinos, papiloso-pilosas en Paspalum am-
modes, P. erianthoides y P. paucifolium. La pilosi-
ser homogénea, en P ammodes, P.
erianthum, P. paucifolium y P. guttatum,
densa en los márgenes de las brácteas, como en P.

dad puede
o más

erianthoides. Los pelos alcanzan hasta 5 mm de
largo en P. guttatum y entre 1—3.5 mm en el resto
de las especies. La gluma inferior se halla ausente,
ocasionalmente se la encuentra en espiguillas ais-

adas en una misma inflorescencia en P. ammodes,
P. erianthoides y P. erianthum.

La gluma superior y lemma inferior son subigua-
les, tan largas como la espiguilla en Paspalum
erianthum y P. paucifolium, y subiguales o la gluma
superior es ligeramente más corta, dejando libre el
dorso apical del antecio, en P. ammodes y P. eriant-
hum. En P. guttatum la gluma superior es tan larga
y la lemma inferior ligeramente

а gluma superior es 5-nervia, con un

como la espiguilla

más corta.
nervio central y los restantes marginales y próximos
entre sf.
3 йү Ырыа
5-nervia, los nervios poseen una distribución sim-
ilar a la hallada en la gluma superior. La pálea
inferior y flor inferior están ausentes en las especies

de Eriantha.

La lemma inferior es (3—)5-nervia, cuando

ANTECIO SUPERIOR
Textura

En las especies del grupo Eriantha de Paspalum
los antecios son elipsoides, de 2.3—4.5(—5) mm de

228

Annals of the
Missouri Botanical Garden

largo y 1-1.9(-2) mm de ancho, cartilaginosos y
pajizos. La lemma y pálea poseen la cara abaxial
finamente papilosa, en P. ammodes у P. paucifo-
lium, o papilosa en las restantes especies. La su-
perficie del antecio superior está compuesta de cé-
lulas largas rectangulares, más de tres veces más

argas que anchas, con las paredes anticlinales lon-
gitudinales y transversales onduladas (Fig. 1F). La
lemma posee los márgenes enrollados y cubre las
2/3 partes de la superficie de la pálea, encerrando
el ápice de la misma (Fig. LA,

Ornamentación del antecio superior

Los antecios presentan papilas distribuidas re-
gularmente sobre la cara abaxial de la lemma y
pálea, cuerpos de sílice o micropelos. Las papilas
son simples, una por célula, excéntricas, próximas
a la pared transversal distal (Fig. 1А—С, F) o ve-

rrucosas, las cuales presentan 3-5 verrugas en
cada papila, en la pálea de Paspalum guttatum
(Fig. 1D, E). Los cuerpos de sílice son halterifor-
mes a ligeramente cruciformes (Fig. IF), exfoliados,
dispuestos hacia los márgenes apicales de la lemma
y pálea. Micropelos son frecuentes en la zona api-
cal de la pálea junto a los bordes de la lemma (Fig.
LA y D) y en el 1/3 superior de la lemma (Fig. 1B,

C). Los micropelos son bicelulares, fusiformes, del

3

tipo “panicoide”, con la célula basal de paredes
engrosadas y la apical de paredes delgadas, ambas
de igual tamaño o la distal dos veces más larga
(Fig. 1C). Se observaron ocasionalmente macrope-
los unicelulares, largos y tiesos hacia el ápice de

a lemma y pálea en P ertanthoides y P. paucifo-
lium.

DISTRIBUCIÓN GEOGRÁFICA Y ECOLOGÍA

Las especies de Eriantha habitan desde el sur
de México y Centroamérica hasta el noreste de Ar-
gentina y norte de Uruguay. La mayor concentra-
ción se halla en Sudamérica, particularmente en
Bolivia, Paraguay, Argentina, Uruguay y sur de
Brasil, donde crecen las cinco especies del grupo.
Las especies del grupo Eriantha crecen desde el
nivel del mar hasta los 1700 m, en suelos arcillo-
sos, arenosos o rocosos; P erianthoides es frecuente
en bañados o cursos de arroyos y ríos. Paspalum
ammodes, P. erianthum y P. guttatum crecen fre-
cuentemente en campos abiertos sujetos a fuegos
periódicos y es común observar en la base de las
plantas restos de vainas persistentes y fibrosas; la
persistencia de estas vainas está probablemente re-
lacionada con la protección de las yemas frente a
factores ambientales adversos y la adaptación de
las plantas a los fuegos frecuentes.

DISCUSIÓN

De acuerdo con los caracteres morfológicos
enunciados, las especies de Paspalum del grupo
Eriantha se caracterizan por incluir plantas peren-
nes, cespitosas a rizomatosas, con cañas simples,
con hojas predominantemente basales, espiguillas
elipsoides, solitarias o en pares, pilosas, con pelos
sedosos, antecio superior cartilaginoso, pajizo, pa-
piloso, con el ápice de la pálea encerrado por su
correspondiente lemma y cariopsis con hilo elfpti-
CO,

Se distinguen dentro de Eriantha 2 subgrupos:
el primero de ellos está formado por Paspalum am-
modes y Р guttatum, ambas especies con espigui—
llas solitarias, distribuidas en 2 series. Paspalum
erianthum, P. erianthoides y P. paucifolium forman
un segundo grupo caracterizado por sus espiguillas
en pares (o la inferior abortada) distribuidas en 4
series, en ocasiones en 2 series.

Eriantha se ubica dentro de Paspalum junto a
otras especies con espiguillas pilosas, como las del
subgénero Ceresia y los grupos Bertoniana y Fas-
ciculata.

El subgénero Ceresia de Paspalum incluye 25
especies que habitan desde México hasta la Argen-
tina, Uruguay y sur de Brasil, y se caracteriza por
incluir plantas perennes (con unas pocas especies
anuales), con láminas rígidas, filiformes a lanceo-
ladas, inflorescencias con | a varios racimos, raquis
manifiestamente alado, membranáceo a hialino, de
0.8-10 mm de ancho, espiguillas pilosas y antecio
superior hialino a membranáceo, con el ápice de la
pálea libre (Denham et al., 2002); sus especies cre-
cen usualmente en lugares abiertos y secos como
sabanas, campos rupestres y cerrados.

El grupo Bertoniana (Chase, inéd.) incluye 2 es-
pecies, Paspalum bertonii Hack. y P. lilloi Hack.,
con una distribución restringida al sur de Brasil,
este de Paraguay y noreste de Argentina. Ambas
especies de este grupo crecen en ambientes hú-
medos, sobre pendientes y suelos rocosos en már-
genes de ríos, cascadas o saltos; las plantas poseen
el antecio superior abierto en su extremo, cariopsis
con hilo linear y las láminas foliares con costillas
adaxiales marcadas.

El grupo Fasciculata de Paspalum (Chase, 1929)
está integrado por una única especie, P. fascicula-
amplia distribución desde
Brasil,
Argentina. Paspalum fasciculatum se

tum Willd. ex Flüggé. de
México y América Central hasta Bolivia,
Paraguay v
halla relacionado a Eriantha por la forma de la es-
piguilla, largamente elipsoide, con los márgenes
papiloso-pestañosos. Paspalum fasciculatum se dis-

tingue por incluir plantas robustas, rastreras, arrai-

Volume 91, Number 2 Morrone et al. 229
2004 Paspalum Grupo Eriantha

Figura ои fías de antecios supe riores de Paspalum. AG. Paspalum т y С de Regnell s.n..
B Ps "iem 2779). ntecio superior, visto del lado de la pálea. —B. Antecio Super rior visto del lado de la lemma.
—C. Detalle de la lemma mostrando pi pilas simples y micropelos bice lular 8. D- К guttatum (de Semir et
al. 375). —D. Ápice del antecio superior visto del lado de la pálea. — Detalle de la pálea mostrando papilas

compuestas. —F. Detalle de la lemma mostrando papilas simples y cuerpos pu sílice.

230 Annals of the
Missouri Botanical Garden
gadas y densamente ramificadas en los nudos in- nado, terminando en una prolongación estéril o en

feriores y medios, con inflorescencias flabeladas y
por habitar a lo largo de márgenes de ríos y arroyos
donde forman embalsados.

Paspalum rufum y P. durifolium, especies res-
ruguay y Ar-
gentina, fueron tratadas por Chase (inéd.) junto con

—

tringidas al sur de Brasil, Paraguay, Û

especies de Eriantha básicamente por compartir es-
piguillas pilosas. No obstante, en el presente tra-
tamiento se considera que ambos taxones no mues-
tran afinidades con las especies aquí tratadas en el
grupo Eriantha. Así, Paspalum rufum incluye plan-

tas robustas, con hojas planas y cortantes, inflores-

cencias truncadas y antecios castafio claros, carac-
teres. por los cuales fue reubicada en el grupo
Virgata de Paspalum por Barreto (1954), criterio
seguido más recientemente por Gomes (1995) y Go-
mes y Monteiro (1996). Paspalum durifolium, que
comprende plantas robustas, hasta de 2 m de alto,
con láminas rígidas, planas a plegadas y cortantes,
con inflorescencias piramidales y antecio estramí-
neo, fue incluida en el grupo Quadrifaria de Pas-
palum por Barreto (1966), Gomes (1995) y Gomes
y Monteiro (1996).

CLAVE PARA DISTINGUIR ERIANTHA DE GRUPOS AFINES
DE PASPALUM EN AMÉRICA

l. Raquis foliáceo, aplanado E 2
1'. Raquis triquet ro x 8
2(1). Antes мо superior hialino a membranác ео, оса-

rupestres, cerrados, sabanas

—

secos, а
у tens ‘Tas rocosa . subg

ә,

2'. Antecio superior euer een con ápice de la
pálea cubierto por los márgenes de la lemma;
inflorescencias flabeladas: cañas con menus
esponjosa; plantas de lugares hümedos, a lo lar
go de inii nes de arroyos y ríos

Ceresia

— Grupo dad 'iculata
3(1). ere "clo npe rior rabia 'rlo en su ápice; cariopsis
con hilo linee ; láminas con M foliares
marcadas мро Bertoniana
J'. Antecio superior cerrado en su ápice: caric opsis
con hilo elíptico; láminas sin costillas foliar
marcadas Grupo Eriantha

TRATAMIENTO TAXONÓMICO
Paspalum grupo Eriantha

Plantas perennes, cespitosas a rizomatosas, con
cañas simples. Lígulas membranáceas. Láminas
lanceoladas a lineares, planas a plegadas o filifor-
mes, de pilosidad variable. /nflorescencias termi-
nales, solitarias, formadas por 2-11 racimos, oca-
ascendentes о

sionalmente un racimo solitario.

adpresas; raquis de los racimos triquetro o apla-

una espiguilla; espiguillas solitarias o en pares, bi-
o tetraseriadas, dispuestas unilateralmente sobre
los racimos; pedicelos breves. Espiguillas elipsoi-
des a largamente elipsoides, plano-convexas, pilo-
sas. Gluma inferior ausente. Gluma superior 5-ner-
via. Lemma inferior glumiforme, (3—)5-nervia.
Antecio superior elipsoide, cartilaginoso, pajizo, ce-
rrado en su ápice, papiloso, con micropelos bice-
lulares hacia el ápice de la lemma y la pálea. Ca-
riopsis con hilo subbasal, elíptico; embrión 4—% del

argo de la cariopsis.

Grupo integrado por 5 especies americanas, dis-
tribuidas desde México hasta el noreste de Argen-
tina, sur de Brasil, Paraguay y Uruguay (se presenta
una lista de estas especies en el Apéndice 1; un
índice de nombres científicos se encuentra en el

Apéndice 3).

CLAVE PARA DISTINGUIR LAS ESPECIES DEL GRUPO
ERIANTHA
|l. Espiguillas solitarias |. ia -
1“. Espiguillas en pares, en oc pera la inferior

reducida o abortada (pero los pl

en pares) |... aa en 3
2(1). Racimos 2, raro 1 6 3, subconjugados; raquis

de los racimos cortamente alado, de 1-1.8 mm

de ancho; lígula de 0.2 mm de largo; espiguillas

elipsoides de 4-5 mm de largo, 1.5-2 mm de
ancho, densamente vilosas, con pelos de 4- 4—5
mm de largao 4. * guttatum
2'. шыл (1 —)2—6, alternos; raquis de los raci-
mos triquetro, de О. nm de ancho; lígula
de 0.4—0.6 mm de lar ae largamente
elipsoides, de 2.4—3.8 mm de largo, 1-1.2 mm
de ancho, er аай con i don de 1-2 mm de
argo oo 1. Р. ammodes
Láminas filiformes, macizas; inflorescenc las su-
bespiciformes, de 1-1.5 em de ancho; raquis
de los racimos кой. de 0.4—0.5 mm de an-
cho 2 P. erianthoides
Láminas lineares o linear-lanc 'eoladas, planas a
involutas; inflorescencias no subespic iformes, de
1-6(-10) em de ancho; raquis de los racimos
aplanado, de 0.5-1.3(-1.5) mm de ancho
deis con rizomas horizontales, viajero
ados; vain > predominantemente basales,
уе de сабо en la base; lami
dominantemente basales, las ER redu-
s 2—4. pauc suai
Plantas de rizomas de entrenados с cortos, d
s basales

—

ы

>
=
w
—

cidas; racimo

A

, laciniadas; láminas basales е
aldag: a lo largo de las cañas; rac imos 52
3. P. ne

1. Paspalum ammodes Trin., Gram. Panic.: 120.
1826. TI
pr. Tejuco”, G. H. von Langsdorff s.n. (holótipo,
LE-TRIN-0415.01!, fotos, KI, SI!; isótipo, US-

PO: Brasil. Minas Gerais: “in arenosis

Volume 91, Number 2 Morrone et al. 231
2004 Paspalum Grupo Eriantha

no 100 50 80 79 LJ 0 E

Nie?
D

pt > Y
1 E

A Р ammodes
% P erianthoides

S SE \ ES
| we 7 |
LIK ABST >

P»

? 200 400 600 800 1000 km
0 100 200 300 400 500 miles
Prepared by Hendrik R. Rypkem:

Figura 2. Distribución de Paspalum ammodes y P. erianthoides.

294.1973!; probable isótipo, L. Riedel 969, B!). barbados a glabros. Vainas más cortas que los en-
Figura 3. trenudos, predominantemente basales, comprimi-

Paspalum sordidum Hack., Oesterr. Bot. Z. 51: 197. 1901. das, aquilladas, las viejas ana adi laciniadas,

TIPO: Brasil. Goiás: Rio Corto. 21 Nov. 1806, 4. Е fibrosas, glabras a densamente hirsutas, con los
‚ Glaziou 22472 (lectótipo, designado por Zuloaga Márgenes glabros a ciliados; lígulas breves, de 0.4—

& Morrone (2003: 515), Wh isótipos, K!, Pl. US-

555444]. US-28560031, foto, SI’). | presente, cuando presente fomada por largos pelos

Paspalum diamantinum Swallen. Phytologia 14: 368.
1967. TIPO: Brasil. Minas Gerais: Diamantina, Serra
le San Antonio, 1200-1300 m. 27-30 dic. 1929, А.

Chase 10401 (holótipo, US no visto: isótipo, MO- 0.2-0.3 em de ancho, las superiores reducidas, fal-
1002695!).

Paspalum canum Sohns, Mem. New York Bot. Gard. 9:
256, f. 6. 1957. TIPO: Brasil. Roraima: Rio Branco,
frequent along stream course E slope of Serra Ma-
rico, 1100 m. 16-18 dic. 1954, B. Maguire & C. la vaina, el ápice agudo a subulado, los márgenes

debe же 40349 (holótipo, US-2182187!; isótipos, Kl. escabrosos, glabros, los basales pestañosos. Pedún-

ót pos 0.6 mm de largo, glabras; pseudolígula ausente o

т
ES

blanquecinos hasta de 2 mm de largo: cuello glabro

a piloso; láminas lineares, de 3-25 cm de largo,
cadas, plegadas o planas, predominantemente ba-
sales, glabras a esparcidamente hirsutas, de base

atenuada, continuándose imperceptiblemente con

culos exertos, hasta de 25 em de largo, cilíndricos,

Plantas perennes, con rizomas breves, rígidos: — glabros: inflorescencias terminales, de 2.4-10 em de
cañas de 20-70 em de largo, 0.2 cm de diámetro, largo. 1-4 ст de ancho; eje principal de 14 em
erectas, paucinodes; entrenudos 2-3, de 7-25 em Че largo, anguloso, glabro, liso a escabroso; pulví-
de largo. cilíndricos a comprimidos, huecos, gla- nulos largamente pilosos, con un mechón de pelos
bros а esparcidamente pilosos; nudos densamente — blanquecinos: racimos 2-6, raro un racimo solita-

232

Annals of the
Missouri Botanical Garden

2
—̃ —

hem come.

PE

=> y

„5 A ——

Se
8 “e

A. Habito. —B. Detalle de la герїбп ligular, cara externa.
Espiguilla vista del lado de la

Figura 3

Paspalum ammodes (de Rojas Ad

TRE de la región cin r, cara interna. —D.

gluma superior. spiguilla vista de 1 lado del ña lemma inferior. —G. Antecio superior visto del lado de la lemma.
—H. Antecio superior visto del lado de la pálea.

talle de una pore ión de racimo. —E.

Volume 91, Number 2
2004

Morrone
1 ram Eriantha

rio, ascendentes, alternos, divergentes del eje prin-
cipal, terminando en una espiguilla desarrollada,
en ocasiones vestigial; raquis de los racimos de 2—
8 em de largo, 0.4-0.6 mm de ancho, triquetro,
sinuoso, verdoso o con tintes violáceos, con la cara
adaxial glabra, las restantes caras hispídulas, los
márgenes escabriúsculos; pedicelos solitarios,
breves, hasta de 1 mm de largo, glabros; espiguillas
solitarias, no imbricadas, dispuestas en 2 series.
Espiguillas largamente elipsoides, de 2.4—3.8 mm
1-1.2

obtuso, plano-convexas, pilosas, grisáceo-verdosas

de largo. mm de ancho, de ápice agudo a
o con tintes violáceos o rojizos; gluma superior y
lemma inferior subiguales o la gluma superior li-
geramente menor, membranáceas, homogéneamen-
te papiloso-pilosas, con pelos sedosos de 1-2 mm
de largo: gluma inferior ausente, ocasionalmente

presente, escamiforme, hasta de 1 mm de largo,
enervia; gluma superior tan larga como la espiguilla
o ligeramente menor, dejando libre el dorso apical
del antecio superior, 5-nervia, con un nervio cen-
tral,

elumiforme,

los restantes. submarginales: lemma inferior
tan larga como la espiguilla, 5-nervia:
antecio superior elipsoide, de 2.3-3.5 mm de largo,
1-1.2 mm de ancho, más corto que la gluma su-
perior y lemma inferior o alcanzando el largo de
las mismas, cartilaginoso, pajizo, glabro, finamente
papiloso, con papilas simples; lemma con papilas

regularmente distribuidas y micropelos bicelulares

hacia el ápice, 5-nervia, con los márgenes enrolla-
dos sobre la pálea: pálea de textura similar a la
lemma con papilas regularmente distribuidas y mi-
cropelos bicelulares hacia los márgenes apicales v
2. de 0.4—0.5 mm de largo:

tambres 3, anteras de 1.8—2 mm de largo. Cariopsis

el ápice; lodiculas es-
elipsoide, de 2.7 mm de largo, 1.1 mm de ancho:
hilo elíptico, un poco menos de la mitad de la ca-
riopsis; embrión 1/3 del largo de la cariopsis.

Distribución geográfica y ecología. Crece desde
Venezuela, Guyana (citado por Judziewicz, 1990) y
Brasil hasta Bolivia y Paraguay (Fig. 2). Habita en
campos sobre suelos arenosos o rocosos. o en suelos
húmedos, en zonas de fuegos periódicos, formando
pequeñas matas entre los 0-1600 m s.m.

Nombre vulgar. (Brasil.
Smith et al., 1982).

Paspalum ammodes es afin a P. guttatum, dis-

“Capim-toucetra”

tinguiéndose esta última por sus inflorescencias for-
madas por 2 racimos subconjugados, raro | o 3,
cortamente alados (de 1-1.8 mm de ancho). espi-
guillas imbricadas de 4-5 mm de largo, densamen-
te vilosas, con gluma superior 0.8—1 mm más larga
que el antecio superior, con los nervios laterales

fuertemente marcados y ligula de 0.2 mm de largo.

La gluma inferior se halla comünmente ausente
en las espiguillas de Paspalum ammodes:; ocasio-
nalmente fue observada en espiguillas aisladas de
una misma inflorescencia en los ejemplares Rojas
6316, Chase 10401, Brito 150 e Irwin & Soderstrom
7395, en los que puede ser rudimentaria, escami-
forme a lanceolada alcanzando aproximadamente %4
del largo de la espiguilla.

Paspalum ammodes se asemeja a P. erianthum
por la morfología de la espiguilla, apartándose esta
ültima por tener espiguillas en pares, de mayor ta-
maño [de 3—5(—5.8) mm de largo] y láminas lan-
ceoladas a linear-lanceoladas.

El ejemplar Riedel 969 coleccionado en Brasil,
sin indicar localidad precisa, examinado en el Her-
bario del Museo Botánico Berlin-Dahlem (B) pro-
bablemente corresponda a un isótipo de Р. ammo-
des |para una discusión más detallada sobre las
colecciones realizadas por C. Н. von Langsdorff у

a Riedel y descriptas por C. B. Trinius véase Ren-
voize (1978)

Hackel (1901) al describir Paspalum sordidum
cita dos síntipos coleccionados en Goiás, Brasil,
Glaziou 22477 y 22472,

es selecionado como lectótipo por coincidir con el

de los cuales este último

protólogo de la especie.

Filgueiras (1993) considera a Paspalum diaman-
tinum Swallen un taxón dudoso y menciona que
podría ser conespecífico con P. erianthoides. El
análisis de la descripción original realizada por
Swallen (1967), del material tipo y de un parátipo
citado por este autor (Chase 10347, IS
W).

lidad un sinónimo de P ammodes.

`

permitió verificar que esta especie es en rea-

Material adicit mal To BOL Ivi A. Santa

—
ар)
+
=
=
N
E
"~
C
ET.
2
—
=
P
ер
EA
D
^
LN
2
Un
—
—
=.
e
fe
A
=
ww
=
2
.
И:
ge

ASIL. Bahia: 5
iontas, Zuloaga et p Pe (MO, SI).
/ of 5 1 8 on road to Bras-
landia, Irwin et al. 10635 (US). Goiás: ca. 50 km S of
‘alaponia on road to Jataí, Irwin n ode "rstrom 7. ey (G,
S). Maranhão: Balsas, Oliveira & da Silva 374 (SI).
Minas Gerais: EO x Serra de San 5 s
10347 (BM US, W). Paraná: Jaguariaiva,
16025 (BM. 65 MA. P, SI). Sao Paulo: San José
Morello s.n. (SI). PARAGUAY. Amambay: (
becera Aquidaban, pendiente 5 Amambay, Rojas 6316
с. Caaguazú: campos al E de
, G, K, P, US). VENEZU ELA. Bolívar: Dist. Roscio,
cuenca del Río Arabopó, aprox. 5 Km de la frontera con
el Brasil, Huber & Alarcón 10505 (MO).

Dis-

c cC
—

Dusén

dos

'

Campos,

Caaguazú, Balansa 71

2. Paspalum erianthoides Lindm., Kongl. Svens-
ca Vetensk. Handl. 34: 6, tab. ТОВ. 1900.
TIPO: Paraguay. Guairá: Villa Rica, 10 Oct.
1874. B. Balansa 72 (holótipo, S no visto: isó-

234

Annals of the
Missouri Botanical Garden

tipos, BM!, G!, K!, LE!, P!, foto, SI!, US-

2854688!). Figura 4.

Paspalum чеш ed Ark. Bot. 9: 5 . 1910. TIPO: =
3, P.

sil. Paraná: Curitiba, in эк dosis, 29 Nov. 19(
K. H. Dusén 2331 (holó lót „WI. йа. BM!, p -
Mt US-285467 30.

Plantas perennes, formando densas matas, con
rizomas robustos, de entrenudos cortos, verticales,
cubiertos por catáfilos seríceos, con pelos sedosos,
pardo-rojizos; cañas de 80—150 cm de alto, 0.2-0.4
cm de diámetro, erectas, paucinodes, glabras, en-
trenudos de 15—45 cm de largo, huecos; nudos
comprimidos, castafios a negruzcos, glabros. Vainas

15-25 cm de largo, predominantemente basales,
aquilladas, las basales seríceas hacia la porción
distal, con pelos largos, adpresos, pardo-rojizos ha-
cia la región ligular, vainas apicales glabras a pi-
losas, con pelos blanquecinos hacia la región li-

ular, el resto de la superficie glabra, los márgenes
cortamente ciliados a glabros; lígulas de 1-2 mm
de largo, glabras, castafias; pseudolígula presente,
con largos pelos por detrás en la base de la lámina,
pardo-rojizos; cuello densamente glabro a piloso,
con pelos pardo-rojizos; láminas filiformes, de 30—
60 cm de largo, 1-2 mm de ancho, predominan-
temente basales, reducidas hacia el ápice de las
cañas, rígidas, macizas, glabras, de base atenuada
y ápice pungente, los márgenes glabros, pestañosos
hacia la base. Pedúnculos largamente exertos, hasta
de 50 cm de largo, cilíndricos, glabros; inflorescen-
cias terminales subespiciformes, de 6-25 em de
largo, 1-1.5 em de ancho; eje principal de 5-19
cm de largo, aplanado, glabro; pulvínulos glabros o
con unos pocos pelitos tiesos; racimos 3-11, ad-
presos al eje principal, alternos, los superiores pró-
ximos, terminando en una espiguilla desarrollada;
raquis de los racimos de 1-8 cm de largo, 0.4—0.5
mm de ancho, triquetro, flexuoso, glabro, liso; pe-
dicelos desiguales, hasta de 2 mm de largo, esca-
briúsculos; espiguillas en pares, imbricadas en 4
series, densamente dispuestas a lo largo del raquis
de los racimos. Espiguillas largamente elipsoides,
de 4-5 mm de largo, 1.5-2 mm de ancho, de ápice
agudo, plano-convexas, largamente pilosas en los
márgenes, verde pálidas y con tintes cobrizos; glu-
ma superior y lemma inferior subiguales, membra-
náceas, con los márgenes papiloso-pestañosos, con
pelos blanquecinos, sedosos, hasta de 2.5 mm de
largo, el resto de la superficie glabra a cortamente
pilosa en la porción central; gluma inferior ausente,
ocasionalmente presente hasta 1/2 del largo de la
espiguilla, pilosa; gluma superior tan larga como la
espiguilla, 5-nervia, con un nervio central y los res-
tantes próximos a los márgenes; lemma inferior glu-

miforme, tan larga como la espiguilla, 5-nervia; an-
tecio superior elipsoide, de 3.9—4.5 mm de largo,
1.6-1.9 mm de ancho, 0.5 mm más corto que la
gluma. superior y lemma inferior o alcanzando el
mismo largo, cartilaginoso, pajizo, papiloso, glabro
o con macropelos largos, tiesos hacia el ápice de
la lemma; lemma con papilas simples, distribuidas
regularmente y micropelos bicelulares, 5-nervia,
los márgenes enrollados sobre la pálea; pálea de
textura similar que la lemma, con papilas simples
distribuidas regularmente y con micropelos bice-
lulares hacia los márgenes apicales; lodículas 2, ca.
0.4 mm de largo; estambres З, anteras de 2.4-3
mm de largo. Cariopsis no vista.

Distribución geográfica y ecología. Habita en
en el sur de Brasil (Paraná y Santa Catarina), Para-
guay Oriental (Amambay, Central y Guairá) y el
noreste de Argentina (Corrientes y Misiones) (Fig.
2); crece frecuentemente en bañados, en márgenes
de cursos de arroyos y ríos desde el nivel del mar
hasta los 1000 m s.m.

Nombre vulgar. “Maceza-do-Banhado” (Brasil,
Smith et al., 1982)

Paspalum erianthoides es morfológicamente
similar a P. erianthum y P. paucifolium, especies
con las que comparte espiguillas largamente elip-
soides y de similar tamaño, con gluma superior y
lemma inferior largamente pilosas hacia los már-
genes. Paspalum erianthoides se distingue por sus
inflorescencias subespiciformes y hojas filiformes,
macizas (vs. inflorescencias abiertas y hojas linea-
res a lanceoladas en P. erianthum y P. paucifolium).
2 5 adicional examinado. ARGENTINA. Cor-
заніо toms! Garruc thos, Burkart 19732 (SI);

ta Na A km antes del Arroyo

), SI). Misiones: i
técnica, prs 28759 (SI
2. un. Teixeira Soares, Río das ree
Had hbach 15356 (К, US); Capáo da Imbuia, Dombrowski
2105 (K). Santa Catarina: Mun. Abelardo Luz, 8-12 is
N of Abelardo ле Smith & Klein 13323 (К, P, US): Mur
Curitibanos, 5 km N of Curitibanos, Smith & Klein 15489
K, P, US dyes C ‘атро Ere, 6 km W of Campo Ere, Au
& Klein 1 1368 0 (K, MO, US). PARAGUAY. Amambay:
= Sierra de Amambay, Hassler 11665 (G, US iS):

regione ‹ логі
G

soil alongo Aceite-i cree 9 (MO).
entral: Prope Sapucay, кы 12906 (BM. N US).

3. Paspalum erianthum Nees ex Trin., Gram.
Panic.: 121. 1826. TIPO: Brasil. Minas Gerais:
Lagoa Santa, Oct., C. H. von Langsdorff s.n.
(holótipo, LE-TRIN- 0450.03!; isótipos, LE!,
US-2854690!; probable isótipo, L. Riedel 724,
P!, foto, SI). Figura 5.

Volume 91, Number 2 Morrone et al. 235
2004 Paspalum Grupo Eriantha

1mm

1 mm

шш |

шш |

1 mm

VAN 8 ў _ aN E -— i d
( 3 PIER. 95 | )
Figura 4. Paspalum erianthoides sein Hassler 10673). —A. Hábito. —B. Detalle de la región ligular. —C. Detalle

de una porción de racimo. —D. iguilla vista del lado de la gluma superior. —E. Espiguilla vista del lado de la
G. Antecio superior visto del lado de la pálea.

lemma inferior. —F. Antecio superior visto del lado de la lemma.

236

Annals of the
Missouri Botanical Garden

Sec

AS

guilla vista del lado de la lemma inferio Antec
G. Са lariopsis, vista escutelar

ira 5.
guma superior.
— .

superior. ntec
(A, de Hassler 11924; B-H, de Hassler 107650

—D.

cio 5 rior visto del lado de la pálea.
1.)

ado de

la lemma

а ie —A. Habito. —B. Detalle de : re gión ligular. —C. Espiguilla vista del lado de la
cio superior visto de
—H. Cariopsis, vista hilar.

Volume 91, Number 2
2004

Morrone et al.
Paspalum Grupo Eriantha

116. 1826.
| rasil. inas Gerais: “in graminosis subhu-
midis S. da Lapa”, dic. 1824, G. H. 1
s.n. (holótipo, LE-TRIN- көт у isótipos, B!, LE
fragmento US-2855985! ex LE,
Riedel 189, K!
„е очага Nees, Fl. Bras. Enum. Pl.

. hom. illeg. TIPO: Brasil. Sin localidad. " Se-
je 5 (lec oo " signado por nerd & Mo-
rrone re 00), Bl; isdtipos, E fot , P!, US-
952 poe 7505!, US- 1441 5261).

жш a Nees v var. strictum Döll, in Martius,

Fl. Bras. 2(2): 70. 1877. TIPO: Brasil. Minas Gerais:

Caldas, А. F. Regnell 111-1336 (lectótipo, aquí desig-

nado, MI: isótipos, G!, US-2854689!, US- 1649820! ).

Р, ju album Swallen, Phytologia 14: 367. 1907.
PO: Br

Paspalum sanguinolentum Trin., Gram. Panic.:
TIPO: Br

robable isótipo, р.

Е

Brasil. Minas z rais: Кичи, Serra Че
E Antonio, 1200—1300 1 —30 dic. 1929, 4.
Chase 10397 a ret 8 foto. Sl: is6-

lipo, SID.
кек involutum Swallen, Phytologia 14: 368. 1967.
PO: Brasil. Minas Gerais: Diamantina, Serra de
) Antonio, 1200-1300 m, 27-30 dic. 1929. 4.

Chase 10400 (holótipo, US-1500757!, foto, SI!).
Paspalum perg Swallen, P hytologia 14: 309. 1961.
TIPO: sil. Minas

Gerais: a. near

Капа, D 10-1200 m, 6 jan. 2
(holótipo. US-1500690!, foto. SIN isótipo. US-
305237).
8 rigens Swallen, Phytologia 14: 309. 1907.
TIPO: Brasil Minas Gerais: 5-10 km M

са ү de S JO m, 27-30
dic. 1929, A. Chase 10442 (holótipo, US-1500:390!,
foto. SIN.

8 intosum Swallen, Phytologia 14: 370 17770
TIPO: Brasil. Minas Gerais: Hargreaves, 1350-140
m. 21-22 dic. 1929, A. Chase 10268 1/2 o

5014331).

Papa dem haughtii Swallen, Phytologia 14: 370. 1907.

TIPO: Colombia. lapin e Los Llanos, ca. 60 km S

00° E of Orocué, ca. 150 m. 19 abr. 1939, O. Haught
2771 (holótipo. US- 17008221. foto, SI*: isótipo. COL-
4644).
Paspalum sericatum Swallen, Phytologia 14: 371. 1967.
TIPO: Br Minas Gerais: Serra do Cipó, 110 km
NE of Belo Horizonte, Chapeo de б de Sol,
1000-1100 m. 28 mar.—l abr. 19 . Chase 9213
O US-1255284!, foto, E. dud MO-
930€
Paspalum. ota Swallen, Phytologia 14: 372. 1967.
TIPO: Bras sil. е Gerais: Hi irereaves, 1350-1400
А. Chai 10268 (holótipo, US-
1501432!, foto. a ёр; US-1501401!, foto. SI).
Се trichoides R. Guzman, Phytologia 51: 468.
TIPO: México. Oaxaca: in vicinity of San Juan
1450-1500 ft., 1 —24 June 1985. E. W.
2735a] (alot, US-

Guic a oi.
Velson 2734a [error por
95220!)

Plantas perennes, con rizomas horizontales de
entrenudos cortos, rígidos, cubiertos por catáfilos
densamente pilosos, con pelos amarillos, adpresos:
cañas de (20-)50-130 em de alto, 0.2-0.4 cm de
diámetro, erectas, de base engrosada, subbulbosa:
entrenudos 2-8, de 6-35

primidos, glabros, estriados: nudos glabros a den-

cm de largo, huecos, com-

von m

samente pilosos, con pelos patentes. blanquecinos.
Vainas de 7—25

vilosas o híspidas, con pelos blanquecinos, adpre-

em de largo, aquilladas, glabras a

sos, los márgenes pestañosos: lígulas breves, de
0.4-0.8 mm de largo, castañas, pseudolígula au-
sente; cuello glabro a piloso; láminas lanceoladas
(0.1—)
0.3—1.6(-2) em de ancho, planas o involutas, as-

linear-lanceoladas, de 4-30 cm de largo.
cendentes, distribuidas a lo largo de las canas o
predominantemente basales, verdosas o con tintes
purpúreos, glabras a densamente vilosas o híspidas
en ambas caras, con pelos cortos, a cortamente pi-
losas en la cara adaxial y glabras en la abaxial, de
base redondeada a angostada en las láminas infe-

РА

riores, formando un pseudopecíolo rígido, el ápice
agudo. los márgenes escabritisculos a pestañosos
hacia la base о en toda su extensión. Pedúnculos
largamente exertos, hasta de 50 ст de largo, cilín-
dricos, glabros: inflorescencias terminales estrechas,
1—6(-10) em de ancho: eje

principal de 2.5-13 ст de largo, anguloso. glabro

de 5-20 cm de largo,

a esparcidamente piloso, escabriúsculo: pulvínulos
largamente pilosos, con pelos blanquecinos hasta

de 7 mm de largo; racimos 2—10, ligeramente di-
vergentes del eje principal a patentes. alternos a
subopuestos, más o menos distantes, separados a
1-5 em. los basales de 4-12 em de largo, los su-
periores de menor tamaño, terminando en una es-
piguilla desarrollada; raquis de los racimos de 0.5—
1.2(1.5) mm de ancho, aplanado, verde a purpúreo,
elabro o con unos pocos pelitos aislados a hispí-
dulo, con los márgenes escabriüsculos: pedicelos
desiguales, hasta de 2 mm de largo, escabriúsculos,
con pelos dispersos; espiguillas en pares, en oca-
siones la inferior abortada, imbricadas. en 4 series,
densamente dispuestas sobre el raquis de los ra-
cimos. Espiguillas elipsoides a largamente elipsoi-
des, de 3-5(-5.8) mm de largo, 1-2 mm de ancho,
sin los pelos, de ápice agudo. plano-convexas, pi-
losas, con pelos blanco-plateados, la superficie pa-
jiza o con tintes purpúreos a purpúreas: gluma su-
perior y lemma inferior subiguales o la gluma
superior ligeramente más corta, membranáceas, con
los márgenes y la base densamente pilosas, con pe-
los ascendentes o la gluma superior densamente
vilosa en toda su superficie, con pelos blanqueci-
nos, sedosos, plateados, flexuosos o rectos, hasta de
3.5 mm de largo, la lemma inferior cortamente pu-
bescente a glabra en su parte media; gluma inferior
ausente, en ocasiones presente, cuando presente
hasta 3/4 del largo de la espiguilla, enervia o l-
nervia; gluma superior tan larga como la espiguilla,
en ocasiones ligeramente más corta y dejando al
descubierto el ápice del antecio superior, 5-nervia.

con un nervio central, los restantes submarginales:

238

Annals of the
Missouri Botanical Garden

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Figura 6. Distribución de Paspalum erianthum.

lemma inferior glumiforme, tan larga como la es-
pen a, (3—)5-nervia; antecio superior elipsoide, de

8—А(—5) mm de largo, 1-1.5(-2) mm de ancho,
eus mm más corto que la lemma inferior o al-
canzando en largo a la misma, cartilaginoso, pajizo,
papiloso, glabro; lemma con papilas simples, re-
gularmente distribuidas y micropelos bicelulares en
su dorso, los márgenes enrollados sobre la pálea,
5-nervia; pálea de textura similar a la lemma, con
papilas simples distribuidas regularmente y con
micropelos bicelulares hacia los márgenes apicales;
lodículas 2, ca. 0.4 mm de largo; anteras 3, estam-
bres de 2.1-2.8 mm de largo. Cariopsis elipsoide,
de 2.4 mm de largo, 1.1 mm de ancho; hilo elíptico,
1/3 del largo de la cariopsis; embrión 1/2 del largo
de la cariopsis.

Distribución geográfica y ecología. | Habita des-
de el sur de México y Mesoamérica, en Honduras
y Nicaragua, hasta Sudamérica, en Colombia, Vene-
zuela, donde es ocasional, y en Bolivia, Brasil, Par-
aguay, noreste de Argentina y norte de Uruguay

(habiendo sido citada para el Dpto. Artigas de este

último país por Rosengurtt et al.,

1970 y Smith et

al.

‘ig. 6); crece en cerrados y en campos

rupestres, en suelos lateríticos o arenoso,

Nombre vulgar.

Smith et al.,

1982

“Macega-do-banhado” (Brasil,

Número cromosómico.

2n

= 80 (Gould & So-
1967; Norrmann et al., 1994),
Paspalum erianthum es afín a Р. erianthoides
(véanse los comentarios bajo esta última especie),
distinguiéndose esta última por tener hojas filifor-

derstrom,

mes, macizas e inflorescencias subespiciformes,

hasta de 1.5 cm de ancho.

En los ejemplares Glaziou 22589, Irwin et al.
9603 y Harley 10495 se observó la presencia de
gluma inferior en espiguillas aisladas en una misma
inflorescencia; la misma puede ser rudimentaria,
escamiforme a linear-lanceolada, alcanzando en
ocasiones hasta 3/4 del largo de la espiguilla.

Esta especie es marcadamente variable en la
presencia de indumento en las hojas. Así, se ob-

Volume 91, Number 2
2004

Morrone et al.
Paspalum Grupo Eriantha

servaron en el espécimen /rwin et al. 9603 laminas
y vainas densamente vilosas; otros, como /rwin et
al. 9197 y Killeen 1369, presentan vainas glabras
y láminas cortamente pilosas, mientras que en /r-
win & Soderstrom 6807 se hallan vainas glabras e
hirsutas en una misma planta. También es mani-
fiesta la variación en el tamaño de la espiguilla: el
isótipo Langsdorff s.n, depositado en US, posee es-
piguillas de 3.5 mm de largo, algo menores a lo
usualmente presente en esta especie. Asimismo, se
han hallado ejemplares con espiguillas algo me-
y Fil-
gueiras & Zuloaga 2207, los que tienen espiguillas
de 3.4 mm de largo; por el contrario, el ejemplar
Hatschbach 35422 presenta espiguillas de 5 a 5.8
mm de largo. Por otra parte, la disposición de las

nores en los especímenes /rwin et al. 7948

hojas es marcadamente variable, hallándose espe-
cimenes con hojas distribuidas a lo largo de las
cafias y otros con las láminas predominantemente
basales. Es muy probable que estas diferencias se
deban a que han sido coleccionados con posterio-
ridad a la actividad de fuegos, ya que en ellos se
pueden observar sus bases quemadas. Esto podría

tener un efecto diferencial en el crecimiento de las
ow mostrando éstas un hábito diferente.

1 el Herbario del Museo Nacional de Historia
Natural de París (P) se conserva el ejemplar Riedel
724, coleccionado en Brasil, que probablemente
corresponda a un isótipo de Paspalum erianthum
(véanse las observaciones bajo P. pata

Los materiales Gardner 3542 y Glaziou 22569,
que fueron determinados por Hackel como 3
lum brevipilum (en herbario), presentan espiguillas
con pilosidad mas corta sobre la gluma superior y
lemma inferior que lo observado más frecuente-
mente en la especie.

Trinius (1826) describe a Paspalum sanguinolen-
tum y distingue a esta especie básicamente por te-
ner inflorescencias con pocos racimos, espiguillas
distribuidas en 2-3 series, cañas erectas, simples
con hojas basales y de color atrosanguínea. El aná-
lisis del material tipo y de numerosos ejemplares
permitió determinar que no existen caracteres para
considerar a esta especie como un taxón indepen-
diente.

Swallen (1967) describe para el grupo Eriantha
de Paspalum 10 especies, sobre la base de ejem-
plares únicos o de pocos especímenes, estos últi-
mos usualmente de la misma localidad, da descrip-
ciones breves para cada taxón y no indica las
afinidades entre los mismos. Este autor proporciona
una clave para distinguir los taxones sobre la base
de caracteres relacionados con la forma y pilosidad
de las hojas y tamaño de las espiguillas. Como se
indicó anteriormente esta especie es marcadamente

variable en la pilosidad de los órganos vegetativos,
como así también en el tamaño de la espiguilla.
Filgueiras (1993) al tratar las especies descritas por
Swallen, considera que P. mollifolium, P. sericatum
y P. formosulum son indistinguibles de P. sangui-
nolentum y los incluye en la sinonimia de esta úl-
lima especie; mientras que trata a P. rigens, P. in-
tosum y P. haughtii como sinónimos de Р.
ertanthum. Por otra parte, Filgueiras (1993) consi-
dera a P. album como una especie válida e incluye
en su sinonimia a P. involutum; caracteriza a esta
especie por la presencia de nudos pilosos y por
tener pelos en la porción basal de la lámina y la
relaciona con Р. erianthoides por las hojas involu-
tas; sin embargo F. erianthoides se distingue por
sus hojas filiformes, macizas e inflorescencias sub-
espiciformes. En el presente trabajo se considera
que la pilosidad de los nudos y de la lámina son
caracteres indistinguibles de otros especímenes de
P. erianthum; además, el tamaño y forma de las
inflorescencias, pilosidad, forma y tamaño de las
espiguillas y la presencia de base subbulbosa del
ejemplar tipo de P. album no permiten diferenciarle
de P. erianthum.

Guzmán (1982) al describir Paspalum trichoides
спа como material tipo el ejemplar E. W. Nelson
2734a depositado en el herbario US. Al revisar el
material depositado en este herbario sólo se halló
el ejemplar Nelson 2735a, el que coincide con los
datos del protólogo. Por ello es posible que el nú-
mero citado por Gúzman se deba a un error al
transcribir la etiqueta del mencionado ejemplar. El
ejemplar Nelson 2735a, conjuntamente con el nú-
mero 2735 del mismo colector, fueron citados bajo
P. sanguinolentum por Chase (1929), y bajo P
ertanthum por Nash (1912) y Chase (1913).

Guzmán (1982) al describir Paspalum trichoides
P. erianthum), y

—

a relaciona con P. haughtii (=
caracteriza a la especie por tener espiguillas de
color pálido, por la pilosidad poco conspicua de la
por tener brác-

gluma superior y lemma inferior y
leas 3-nervias, caracteres que no permiten diferen-
ciar a la especie de P. erianthum.

(1970) y Smith
et al. (1982) es un forraje apetecido, poco produc-

De acuerdo a Rosengurtt et al.

tivo.

Material adicional examinado. ARGENTINA. Cor-
rientes: Dpto. Santo Tomé, Ruta д. 40, 4 km de Агага
camino a Garr eae coe del R
al. 1802 (MO, Sh. 1 OL
km S de Riberalta, B E del camino Riberalta-Santa LN
Hanagarth & Rosales 149 (LPB, SI). Santa Cruz: Ñuflo
de Chávez, Ea. San Josecito, З km N of Concepción, Kil-
1139 (LPB, MO, SI). BRASIL. Ceara: sin localidad,
1840, Gardner 1888 (G, K, P, US, W). Distrito Federal:
Brasília, Lago Sul, Zuloaga 3836 (SI). Goiás: Serra do

240

Annals of the
Missouri Botanical Garden

Caiapó, ca. 30 km N of Jataí, on road to Caiaponia, Irwin
& Soderstrom 7302 is) › US). Mato Grosso: са. 90 km
` Xavanti & Soderstrom 6809 (B, K, MO, SI,
US). Minas Gera: campos de Itabira, Glaziou 17939 (G,
K, P, W). Parana: Ponta ea Swallen O). Rio
e € sin localidad, 1885, Glaziou 15635 (G, К,Р,

5, W). Sao Paulo: Casa Branca, Chase 10584 (MO, W).
А 0 OMBIA. Meta: 20 km SE Villavicene о, ا‎ 34.
S). HONDURAS. Comayagua: along . CA-5,

E of Siguatepe нр ohl & ес 12039 (0)
Olane ho: Mun. La Unión, ca. 10 mi. E of La Unión along
road to Olanchito, Dadu et al. 35467 (MEXU, MO).
۰ vicinity of San Juan Guichicovi, Nel-
son 2735 (US). CARAGUA. Matagalpa:
Apante Grande, ca. 2 km al 5 de Ni
118 (MO). PARA( ios Aman
e йү. Sierra de Amambay”, йн

VENEZUELA. Barinas: cerc s de Barinas, ca-
rretera a San Si lestie: Ramia 1145 (MO).

—
—

—

4 4

4. Paspalum guttatum Trin., Gram. Panic.: 91.
1826. TIPO: Brasil. Minas Gerais: Barra do
Jequitiba, nov. 1824, G. Н. von Langsdorff s.n.
(holótipo, LE-TRIN-0468.02'; isótipos, LE!,
US-2855317!; probable isótipo, L. Riedel s.n.,
Kl. PI). Figura 7.

Plantas perennes, con rizomas rígidos, de entre-
nudos cortos; cafias de (40—)50—90 cm de alto, 0.2—
0.3 em de diámetro, erectas; entrenudos 2-3, de
15-25 cm de largo, cilíndricos a comprimidos, gla-
bros, huecos; nudos glabros a pilosos, castaños.
Vainas más cortas que los entrenudos, predominan-
temente basales, persistentes en la base, lacinia-
das, fibrosas, protegiendo la base, glabras a hirsu-
tas, los márgenes glabros a pestañosos; lígulas de
0.2 mm de largo; pseudolígula formada por un arco
de pelos densos hasta de 0.5 mm de largo; cuello
glabro; láminas lineares, de 10-30 cm de largo,
0.2—0.4 cm de ancho, planas a involutas, predo-
minantemente basales, reducidas hacia el ápice de
las cañas, las más viejas espiraladas, enrolladas en
la base; láminas con la cara adaxial glabra a hir-
suta, la abaxial hirsuta, de base atenuada y ápice
largamente agudo, los márgenes papiloso-pilosos.
Pedúnculos largamente exertos, hasta de 45 cm de
largo, cilíndricos, glabros; inflorescencias termina-
les, de 3-8 cm de largo, 2-8 cm de ancho; eje
principal nulo; racimos 2, raro 1 6 3, subconjuga-
dos, ascendentes, terminando en una prolongación
estéril con espiguillas parcialmente desarrolladas;
pulvínulos densamente vilosos, raquis de los raci-
mos de 3-9 cm de largo, 1-1.8 mm de ancho, apla-
sinuoso, verdoso a violá-

nado, cortamente alado,

ceo, glabro a hispídulo, aquillado, con quilla
prominente, escabrosa, los márgenes escabrosos;
pedicelos hasta de 1 mm de largo, cortamente pi-
losos; espiguillas solitarias, imbricadas, densamen-

te dispuestas a lo largo del raquis en 2 series. Es-

piguillas elipsoides, de 4-5 mm de largo, 1.5-2 mm
de ancho (sin los pelos), de ápice agudo, plano-
convexas, densamente vilosas, plateadas, con tintes
purpúreos entre los nervios; gluma superior 0.8-1
mm más larga que la lemma inferior, membranácea;
gluma superior tan larga como la espiguilla, con los
márgenes y la porción basal densamente pilosa, con
pelos plateados, sedosos, de 4—5 mm de largo, el
resto de la superficie esparcidamente pilosa, 5-ner-
via, con el nervio central y los 2 laterales fuerte-
mente marcados, los restantes tenues, submargi-
nales; lemma inferior glumiforme, de 3.8-4 mm de
largo, densamente vilosa, 3-nervia; antecio superior
3-3.6 mm de largo, 1.4—1.6 mm de
mm más corto que la gluma superior,

elipsoide, de
ancho, 0.8-1
pajizo, cartilaginoso, glabro; lemma con papilas
simples distribuidas regularmente y micropelos bi-
celulares hacia el ápice, 5-nervia, los márgenes en-
rollados sobre la pálea; pálea de textura similar que
la lemma, con papilas verrucosas distribuidas re-
gularmente, cuerpos de sílice y micropelos bice-
lulares hacia los márgenes apicales; lodículas 2, ca.
0.4 mm de largo; estambres 3, anteras de 2.4-2.6
mm de largo. Cariopsis no vista.

Distribución geográfica y ecología. Crece en
Brasil Central, en el Distrito Federal, Goiás, Mato
Grosso, Minas Gerais y Sáo Paulo (Fig. 8). Habita
en cerrados, en campos o laderas, sobre suelos are-
nosos, arcillosos o entre rocas, preferentemente en-
tre los 300-1600 m de altura.

Paspalum guttatum es afín a P. ammodes por ser
las únicas especies del grupo con espiguillas soli-
tarias, por tener láminas lineares, predominante-
mente basales, y espiguillas elipsoides a largamen-
te elipsoides y papiloso-pilosas (véanse las
diferencias entre estas dos especies bajo observa-
ciones de P. ammodes).

Algunos ejemplares con largos racimos recuer-
dan superficialmente a H eucomum Nees ex Irin.
y la forma de la espiguilla a P. carinatum Humb.
& Bonpl. ex Flüggé, miembros del subgénero Ce-
resia de Paspalum.

En el Herbario del Museo Nacional de Historia
Natural de París (P) y en el Jardín Real Botánico
(K) se halló el ejemplar Riedel s.n., coleccionado
en Brasil, que probablemente corresponda a un isó-
tipo de P. guttatum (véanse las observaciones bajo
P. ammodes).

BRASIL.

Material adicional examinado. Distrito

Federal:

. Goiás: sin localidad, Glaziou 22442 a M,
V.“): N Serra de São Pedro, Glaziou 22467 (K. P
W) ato Grosso: Faz. Urubá Branco, Pires & Silva

Volume 91, Number 2 Morrone e 241
2004 Paspalum ae Eriantha

.
—

SSS =

کے

de 4
\ P"

==

ڪڪ

/
=

V
)
ALS
a
t=
5

M N 22
TN A

— —
—

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—

A
A

B
Figura y? шп шиш ibito. —B. Detalle de la región ligular. —C. Detalle de una pore ión de
racimo. —D. Espiguilla vista del lado de j* gluma superior. —E. Espiguilla € * lado de la lemma inferior. —
Antecio superior visto del lad o de la lemma. —G. Pálea superior, vista dorsal. —H. Pálea superior con lodículas. (A.

B. de Glaziou 22440; C-H, de Chase 10312.)

11322 (US); vicinity of Xavantina, Irwin & Soderstrom
6795 (SI). Minas Gerais: Hargreaves, Chase 10277 (R,
W); Serra da Lapa, Riedel s.n. (P, US). Sao Paulo: Mun.
Botucatu, 18 km N of Botucatu, 14 km E of Sao о
along the Sáo Manuel-Piracicaba hw 5 218—
31872 (MO); Casa Branca, Loefgren 1508 ( » US) Mun.
Itirapina, 6 km NE of 1 0 at e E on Campinas,
Sao Carlos, Skvortzov 69 (K, MO

Paspalum paucifolium Swallen, Phytologia
14: 372. 1967. TIPO: Brasil: sin localidad, F
Sellow 3541 (holótipo, US-1258166!, foto, 51;
isótipos, B!, Р!). Figura 9

d

Plantas perennes, con rizomas horizontales, ar-
queados, viajeros, cubiertos de catáfilos vilosos,
con pelos blanquecinos, adpresos; cafias de 40—100
ст de alto, 0.2-0.3 ст de diámetro, erectas, pau-
cinodes; entrenudos 2—5, de 7-25 cm de largo, ci-
lindricos, huecos, glabros; nudos comprimidos, cas-
taños, glabros a pilosos. Vainas predominantemente
cm de

basales, superpuestas, las basales de 1-:
largo, densamente hirsutas, rodeadas de catáfilas

242 Annals of the
Missouri Botanical Garden
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Prepared by Hendrik R. Rypkema 1
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Figura 8. Distribución de Paspalum guttatum y P. paucifolium.

en la base, las de las cañas floríferas de 5-15 cm
de largo, hirsutas en la porción distal, luego gla-
bras, los márgenes glabros a pestañosos; lígulas de
0.5-1.4 mm de largo, de ápice lacerado, glabras;
pseudolígula ausente; cuello glabro a piloso, cas-
taño; láminas lineares a linear-lanceoladas, de 5—
18 cm de largo, 0.3—0.6 cm de ancho, reducidas
hacia el ápice de las cañas, predominantemente ba-
sales, rígidas, planas, glabrescentes a densamente
papiloso-pilosas en ambas caras, con pelos cortos,
de base redondeada a subcordada y ápice agudo a
subulado, los márgenes escabriúsculos, largamente
pestañosos, con pelos tuberculados, blanquecinos,
hasta de 6 mm de largo. Pedúnculos largamente
exertos, hasta de 30 cm de largo, cilíndricos, gla-
bros; inflorescencias terminales de 4.5-12 cm de
largo, 2-4 cm de ancho; eje principal de 1-6 cm
de largo, aplanado, glabro, escabriúsculo a liso;
pulvínulos largamente pilosos; racimos 2-4, alter-
nos, ascendentes, distantes entre sí, adpresos a li-
geramente divergentes del raquis, terminando en

N
A
[ev]

Volume 91, Number 2 Morrone
2004 aun OM Eriantha

ra a ати paucifolium. —A. Hábito. —B. Detalle de la región ligular. —C. Detalle de una porción de
rac imo. —D. Espigu uilla vista del lado de la gluma aa E. Lemma inferior con estigmas de la flor superior. —

. Antecio superior visto del lado de la lemma. —G. Ant superior visto del lado de la pálea. —H. Cariopsis, vista
escutelar. —I. Cariopsis, vista hilar. (A, de Р Эи 73; B. T de Burkart 26195.

244

Annals of the
Missouri Botanical Garden

una espiguilla desarrollada; raquis de los racimos

e 2-6.5 ст de largo, 1-1.3 mm de ancho, apla-
nado, glabro, verdoso a violáceo, con los márgenes
glabros, escabritisculos; pedicelos desiguales, hasta
de 1.6 mm de largo, escabritisculos a pilosos, con
pelos blanquecinos en los márgenes; espiguillas en
pares, en ocasiones la inferior abortada, dispuestas
en 4 series. Espiguillas largamente elipsoides, de
3.6-5 mm de largo, 1.2—1.8 mm de ancho (sin los
pelos), de ápice agudo a acuminado, plano-conve-
хаз, papiloso-pilosas, plateadas; gluma superior у
lemma inferior subiguales, membranáceas, con los
márgenes y la base largamente pilosos, con pelos
blanquecinos hasta de 3 mm de largo, la gluma con
la región media cubierta por pelos y la lemma con
la región media pubescente; gluma superior tan lar-
ga como la espiguilla, 5-nervia, con un nervio cen-
tral y los restantes marginales; lemma inferior glu-
miforme, 3-nervia; antecio superior elipsoide, de 3—
4 mm de largo, 1-1.2 mm de ancho, 0.5-1 mm más

corto que la gluma superior y lemma inferior, car-

tilaginoso, pajizo, finamente papiloso; lemma con
papilas simples distribuidas regularmente, macro-

pelos y micropelos bicelulares hacia el ápice, los

márgenes enrollados sobre la pálea, 5-nervia; pálea
de similar textura que la lemma, con papilas re-
gularmente distribuidas y micropelos hacia los
márgenes y el ápice; lodículas 2, ca. 0.3 mm de
largo; estambres 3, anteras de 2.4—3 mm de largo,
amarillentas. Cariopsis elipsoide, de 2.4 mm de lar-
go, 1 mm de ancho; hilo elíptico, 1/3 del largo de

a cariopsis; embrión 1/3 del largo de la cariopsis.

Distribución geográfica y ecología. | Habita en
Brasil, Paraguay, Uruguay y Argentina (Fig. 8), fre-
cuente en campos húmedos, en suelos arcillosos,
arenosos o médanos o a lo largo de arroyos.

Nombre vulgar. | "Capim-formiga" (Brasil, Smith
et al., 1982).

Paspalum paucifolium es afín a P. erianthum por
compartir ambas especies espiguillas largamente
elipsoides, papiloso-pilosas y antecio superior pa-

piloso y con micropelos bicelulares hacia los már-
genes apicales. Se distingue de P. erianthum por
poseer la base rizomatosa, con rizomas viajeros, ho-
rizontales, arqueados, cubiertos por catáfilos vilo-
sos, hojas dispuestas en la base rodeadas de catá-
filos, inflorescencias con 2 a 4 racimos, y antecio
superior 0.5-1 mm más corto que la gluma superior
y la lemma inferior.

Swallen (1967) describe a la especie con espi-
guillas solitarias. El análisis del material tipo y de
material de herbario permitió observar que la es-
piguilla inferior del par se halla reducida y los pe-
dicelos se distribuyen en pares. Es frecuente ob-

servar en una misma inflorescencia espiguillas en
pares y otros con la espiguilla superior desarrollada
y la inferior abortada como en Balansa 73 y 4360.

Swallen (1967) al describir. Paspalum paucifo-
lium cita como holótipo el ejemplar coleccionado
por Sellow en Brasil, sin indicar nimero de colec-
cíon. El análisis del holótipo depositado en el her-
bario US permitió verificar que en el ejemplar se
indica claramente que dicho número es Sellow
3541; duplicados de esta colección fueron también
examinados en B y en P.

Material adicional examinado. ARGENTINA. Co
rientes: Dpto. San Cosme, Paso de la Patria, Quarín 3028
(SI); Dpto. Mburucuyá, Estancia Santa María, Pedersen
4552 (MO); Dpto. 5 Lomas de es Pe
dersen 9679 (MO). Entre Rios: Palmar Grande de C pion.
Burkart 20571 (S m ‚ bafiados del Río Mocoretá,
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'ronimo, Fazenda do
1 Barreto 829 (SI); Uruguaiana, Swallen 7643 (MO,
US). PARAGUAY. Ama І nambay, ‘in
campis altis Peguahó", uie 1
Apa und Río de nae Caballero Cué

(BM. G, K). Central: near Villeta
Campo Grande, entre Luque et La Trinidad, ардым 73
G, K, P). Guairá: ltapé, Balansa 73a raguarí:
1882, ea 4360 de i Cui Es-
tane ы us "rito, н 13 CTES). URUGUAY. Arti-
gas: Rio Uruguay rroyo ae es 1 Ezequiel
1970 (CTES); Río EBD y Ayo. Ha-

^).

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—

sin localidad, oct.

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Palma, 5
cumbü, Rosengurtt et al. 10513 (CTI

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оя Las especies afines а и quadri-
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Cialdella, A. M., e & К. О. Zuloaga. 1995. Re-
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num. Her Majesty s ee nie e, London.
Denham, S. S., F. О. Zuloaga & О. Morrone. 2002.
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Ceresia (Poaceae: deo Paniceae). Ann. Missou-
ri Bot. Gard. 89: 337—
J. C. 1877. n. En: C. F. P. Martius (edi-
tor), Fl. Bras. 2(2): 1-358. Munic n Viena, Leipzig.
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Filgueiras, T. S. 1993. Nomenclatural and critical notes

Сой,

3

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l.
Paspalum Grupo Eriantha

on some iini hok species of ا‎ (Poaceae: Pa-
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1994. Paspalum biaristatum (Poa-
from Goiás,

—

niceae). rag
rG. Davidse.
ceae: Paniceae), a new serpentine endemic
ip and the second awned species in the genus. No-

: 18-22.

Сотев, M. I.
nero Paspalum L.,
Brasil. Швеи (Ме
mento de Botánica, Universidade

nas

1995. Estudios Taxonómicos no Gé-
Grupos “Virgata” e “Quadrifaria” no
strado em Botánica), Departa-
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. Monteiro. 1996. As espécies de Paspalum

) dos grupos Virgata e Quadrifaria no Bra-
Tecnol. 39:

€
. (Poaceae)
e ы s e ecologia. Arq. Bio
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Gould, F. W. & Т R. Soderstrom. 1967. 5

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233—

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* Gorts-van Rijn (editor), Flora of the Guianas. Serie
: Phanerogams. Koeltz Scientific Publications. Koe.
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uz. Bolivia. Ann. Missouri Bot. Gard. 77: 125-201
г ану O., К. O. Zuloaga & E. аон. 1995, Revisión
del grupo Racemosa del género Paspalum (Poaceae: Pa-
nicoideae: Paniceae). Ann. Missouri Bot. Gard. 82: 82—

116

Vega & F. О. ae on Revision de las
especies del género Paspalum L. (Poaceae: Panicoi-
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103-138.

.S. S. Denham, S. S. Aliscioni & F. O. Zuloaga.
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Pilger, R 1929. Berme unten zur Systematik der
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228-231.

. 1940. = III. Unterfamilie Panicoideae.
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Pohl. R ^W. & G. Davidse. 1994. mu Рр. 335-
352 en G. Davidse, M. Sousa & A. aater (editors),
Flora Mesoamericana, Vol. 6. eode ‘eae a Cypera-
ceae. Sd pink Nacional Autónoma de México, Méx-
ico, D.F.; Missouri Botanical Garden, St. Louis; The
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Renvoize The genus Panicum Group Lorea
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srg ais Grasses of Bahia. Royal Botanic Gar-

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dens,

1988. dm hbach's Paraná Grasses. Royal Bo-

tanic 8
— — 98. ramis as de Bolivia. Royal Botanic Gar-

dens, "Kew 1

вооа. f Н. R. 1999. Una nueva sección del género
Paspalum L. (Gramineae): Sección Parviflora Rodrí-
guez оса 8: 99-103.

Maffei & P. Izaguirre de
Universidad de

B. Arrillaga de
. Gramíneas Uruguayas.

Rose тш, B.,

ic
P MAN 1978. Paspalum species

of the Serra do А лро (D): A n E the study of
the i can Poaceae. Revista Brasil. г ТЈ 15
— —. 1980 Paspalum species of the Serra

do Cipó (1): " contribution to the s we of the E an

vace € Revista Brasil. Bot. 3: 2-38

Smith, L. y у {. М. y ein. 1982.
rai as. En: n Reitz (editor), Fl. II. Catarine пзе,
"asc. Gram. 85. M v. até 115. Zea: 910-140

Soderstrom, T. H. 1989. " revision T.
the genus p E segregate
diolyra (Poace g Bambusoide: ae: Oly reae). Sunc

łot. 69:

Zu m m

= .

enus aro-

T
=
—
-
—

R. New species of Paspalum. Phyto-
: 358-389.
1826.
botanic ‘a altera, Impensis Academiae Imperialis Seien-
tiarum. Pe чи че (St. Petersburg)
E . Morrone. is Paspalum. Еп Е. О.
шло С. Davidse, T. 5.
. J. Soreng & К. aes wicz Сейте
Catalogus of E w World Grasses (Poaceae): III. Subfam-
a Panicoideae, Aristidoideae, SET ^ an
лу аана Contr. U.S. Natl. Herb. —521
——— — & —— ———. En prensa. Revisión Ps [he
de "horae para América del Sur Austral (: m ntina,
Bolivia, sur » Brasil, Chile, INN y Uruguay). Mo-
nogr. Syst. Bo . Missouri Bot. Gard.
TE "eS ا‎ 2003. Classification
We biogeography а the Panicoideae in the New World.
P. 100 en Fourth International Symposium on Gras
Systematics and Evolution, Claremont, California. | Ab-
stract.

De Graminibus Paniceis. Disertatio

Filgueiras, P.

ecies

APÉNDICE 1.
Lista de especies aceptadas del grupo Eriantha de Pas-
palum.

l. Paspalum ammodes Trin.

2. P. erianthoides Li

3. P. erianthum Nees ex Trin.
4. P. gutt Tri

5.

P. paucifolium Swallen

APENDICE 2. Índice de colectores. Cada espécimen es
ordenado alle ‘ticamente por su primer colector. El (
corresponde a la especie.

Allem 309 (4), 1089 (4),
Archer 4088 (3).
Balansa 71 (1), 72 (2). 73 (5), 73a (5). 4360 (5); Bald-
win 3077 (3); po 829 (5). 887 (5 ; Beck. 20556 (3):
200 21575 (3): Borges 11519 (4): Brito 150 (1); Burch
6 (3); iude E (3). 8005 (3), 8332 (1): irc wn
1922 (2), 20571 (5), 22910 (5), 24722 (5), 2619
Cabrera 28759 (2); Carnevali 3380 (5); Castellano

1117 (4); Altson 7568 (3):

21740 (1); Catal 1 1); Chase 9296 (3). 10226 (3).
10244 (3), 10277 (4), 10307 (4), 10308 (4). pee (4).
10315 (3). 10323 (3). 10327 (3), 10345 (4). 10347 (1).
10414 (4), 10483 (3), 10509 (3), 10512 (3), 10521 (3).

Annals of the
Missouri Botanical Garden

10525 (4), 10559 (3), 10566 (3), 10584 (3), 10605 o
mo (3), 11731 (3), 11901 (3), 12063 (3) ; Chav
648 (1); Cristophel 134 (4

Da 35467 (3); de Campos 113 (3); Dombrowski
2105 (2), 5457 (2), 5650 (2), 6345 (3), 6717 (3); Dusén
1189a (2), 1234a (1), 1354a (3), 2331 (2), 8918 (2), 10413
3), 10885 (2), 13257 (1), 13543a (3), 15669 (3), 16025
(1), 17409 (3), s.n. (3); Dutra 546 (5).

Киеп 1483 (3), 6749 (3), 9044. (3).

Fiebrig 4908 (5); Filgusiras 766 (4), 2207 (3), 2885 (1);
Fonseca 1222 (1); Fróes 30164 (1).

Gardner 1888 (3), 3541 (1), 3542 (3); Glaziou 15635
(3). 16538 (3), 16558 (3), 17373 (3), 17374 (3), 17939
(3), 20556 (3), 20560 (3), 22440 (4), 22442 (

(4), 22469 (1), 22471 (1), 22477 (1), 22478 (1),

(3), 22490 (3), 22491 (3), 22492 (3), 22510 (3 ), 22589
(3), 22608 (3), 22613 (3), s.n. (1); Gottsberger 28-31872
(1), 218-318 b

Hanagarth 149 (3); een 10307 (3), 10495 (3), 15466
(1) ; Hassler 9539 (1), 9742 (3), 10673 (2), 10765 (3),
10765a (3), 11377 (2), 11665 (2), 11924 (3), 11941 (2),
11989 (5), 12906 (2) : ; , Hatschbach 8436 (2), 15356 (2),

33188 ( 3), 35422 (: 3), 48512а (1 D; Heringer 11629 (3
Hoehne 9741 (4); Huber 10505 1).

Irwin 6078 (3), 6685 (3), 6701 (3), 6795 (4), 6807 (3),

6809 (3), 7040 (1), 7302 (3), 7395 (1), 7948 (3), 8231

" 8382 (9) 8383 (3) 8590 06) 9138 (1), 9139 (1), 9163
, 95

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(1 3),

(1 ), 10259 155 10260 (1), 10330 (1), 10332 (3), 10398

(1), 99 (1), 10635 (1), 10653 (1), 10890 (3), 10891

(3), a0. Ah 9 3), 23560 (3); Izaguirre 1970 (5).
ly 1726 (3); Jonsson 1234a

bns 1139 (3), 1194 (3), 1369 (2 3), 2191 (3), 2781
(1), 2779 (3), 2786 (1), 7039 (3), 2158 (3), 7210 6; 7743
ves Kilip 34323 (3); Klein 3255 (2), 3336 (2), 3728 (2),

2 (1); Kral 75196 (3), 75910 (3).

jota 149 (3), 193 (3), 1508 (4), 3818 (3).

Macedo 1388 (1), 1401 (3), 27 іа (3); Martius s.n. (3);
Mattos 8340 (3), 8500 Sh Mimura 558 (3); Mizoguchi
2602 (3); cv n. (1), s.n. (3); Morrone 1802 (3); Mos-
tacedo 2183

Nelson ras (3); Nicora 5746b (5).

Occhioni s.n. (3); Octacilio s.n. (4); Oliveira 374 (1),

Pedersen 4503 (5), 4552 (5), 9503 (5), 9679 (5); Pires
2842 (3), 11322 (4); Pohl 5051 (3), 5061 (3), 12039 (3),

Quarín 3028 (5).

Ramia 1145 (3); Ramos 178a (3); Regnell s.n. (3); Ren-
voize 3066 (2); Riedel 724 (3), 849 (4), 1135 (3), s.n. (4);
Rojas 6316 (1), 13164 (5) ; Rondón 2136 (3), 2147 (3
ша 10513 (5); Royo Pallarés 178 (5); Rúgolo 1687

ES 10337 (2); EP s.n. (3); iin 375 (4); Sen-
dulsky 393 (3), 437 (1), 452 (1); Shaw s.n. (3); Skvortzov
(4); Smith 8278 (2), 929 (2). 11628 (2), 13323 (2),
13680 (2), 15482 (2), 15630 (2), 15662 (2), 15674 (2),
15693 (2), 15746 (2); Soria 6805a (1); Soza 118 (3); St.
Hilaire 90 (3); Steinbach 3543 (3); Swallen 7117 (5), 7643
(5), 8363 @), 8458 (3), 9162 (5).

Vargas s.n. (3); Viegas 5187 (3), 5953 (3).

Walter 3467 (1); Weddell 2750 (3); Widgren 879 (3),
1149 (4), 1288 (3), s.n. (4); Williams 11873 (1); Wood
13965 (3).

o
Of

—

Zardini 52304 (1), 52369 (2); Z fe 3066 (2), 3234
2), 3836 (3), 4676 (3), 4698 (3),

2 (1).

APENDICE 3.

Indice de nombres c ento ‘0S.

* sinónimos en it:
jus th

РЕ
=

1yris, sección 926

Anachyris, subgénero 226
Axonop us 226
n grupo 228. 230

Ce
Ce

›гегае, sección
eresia, sección 226

eresia, subgénero 226, 228, 230, 240
22

~

Conjugata, grupo
Cymatochloa, secc ión 226
Dilatata, gru 6

E mprosthion, s sección 226
z remachyrion, sección 226

riantha, puo ur 227, 228, 230, 239
n 226

: rianthum, s

Eriole иша. secc "ión 226
Eupaspalum, sección 226
Fasciculata, grupo 228, 230

)
Opisthion, sección 226

P
Р.
P.
P.
na
P.
Р,
Р
Р
Р.

x

: d :
Р. erianthoides 226, 227, 228, 230, 233, 234, 238, 239
Р,
24

Р.
Р.

p]

Pg
P

)
Paspalum 225, TU 997, 228, 230, 239, 240
, 239

album 226, 2

ammodes og 227, 228, 230, 233, 239, 240
bertonii 22

ble, саш 226

сапит

т
vigi 226
devincenzii 226
5 226, 231, 233

' dilatatu

durifolium 226. 230

dusenii
erianthum 226, 227, 228, 230, 234, 237, 238, 239,
1

erianthum var. strictum 237
eucomum ¿
asciculatum 228
5 226, 237

х 227, ns [m 231, 240

=
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ana sler

a й T 237, 239

P. humboldtianum ey

P. intosum 226, 237, 239

P. involu B А 226, a 239

P. lilloi 2

P molijolium 226, 237, 239

P. ovatum <

P. pauc cifolium 226, 227, 228, 230, 234, 242, 244
P. polyphyllum 226

P. rigens 226, 237, 239

P. rufum 226, 23(

P; sanguinolentum 226, hoe 239
P. sericatum 226, 237,

Р, элечи x ei 2

P. trichoides

Pte in s sece scil 226
5 grupo 230

irgata, grupo 230

PHYLOGENETIC ANALYSIS Thomas Haevermans,? Petra Hoffmann, 3
OF THE MADAGASCAN Parr do Ikt Jean Noni Labas,
EUPHORBIA SUBGENUS | |
LACANTHIS BASED ON ITS

SEQUENCE DATA!

ABSTRACT

Euphorbia subg. Lacanthis accounts for more than 70% of the Euphorbia species in ene dh ar. These spiny
succulent plants, with about 80 species endemic to the redes include E. milii (“Crown-of-Thorns”), which is Méca
in the worldwide horticultural trade. The genus was last revised by Boissier in 1862, and the taxonomy of the spiny
succulents is currently much confused. Using DNA sequence deka, phylogenetic oe wil vin subgenus [ааш йз
are clarified and the diversification of Madagascan Euphorbia is examine este
proaches are used to analyze ITS sequence data. The r [
subgenus ile re a ia clade that is not closely related to the n: Ne subg. Lacanthis S. str.,
an exclusively Madagascan group whose basally branc hing lineages comprise species from northern and eastern Mad-

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agascar, a edie the more derive clades show a central and southern ас This s Pom a northern Madagascan
origin for subgenus Lacanthis, with species in the basally branching groups showing small spine-like stipular formations;
qna more recently derived spiny forms, such as E. milii, colonized the rest of the Dad: including the drier southern
par

Ke ey words: DU Euphorbiaceae, Internal ‘Transcribed Spacers, ITS1, ITS2, 5.85, Lacanthis, Madagascar,
molec Шз phylogenetics

The taxonomy of Euphorbia L. has always been ally desirable species). In addition, attempts to as-
problematic due to the sheer size of the group (ca. sess phylogenetic relationships based on morphol-
2000 species) and the tremendous range of mor- ору are confounded by succulence and other
phologies seen among members of the genus. This adaptations to extreme conditions, making it diff-
situation is compounded for the succulent spiny cult to establish homologies for many taxonomically
taxa (hundreds of species worldwide) because spec- important characters. In view of these difficulties,
imens are often fragmentary and poorly preserved, analyses based on an independent data set, such
and many taxa were described from living or spirit as molecular markers, may offer insight into the
specimens that have subsequently been lost. More- evolutionary history of the succulent members of
over, it is often difficult to obtain material because Euphorbia.
export of these plants is subject to restrictions (all The goal of this paper is to clarify the phylogeny
succulent taxa of Euphorbia are listed in CITES of the spiny succulent Euphorbia species in Mad-
appendix I or II. as they include many horticultur- agascar using DNA sequence data, and thus to pro-

! Fieldwork was supported by a National Ge graphic Society grant (6962-01), and was made possible with the
collaboration in Madagascar of ANGAP, CNRE, and FOFIFA. We thank the Missouri Botanical Garden Madagase ar
office in Antananarivo for logistic help. The molecular analyses were conducted both at the Service de Systématique
Moléculaire (C ИҢӘ, FR1541) of the Muséum National d'Histoire. Naturelle (Paris, France) with the support of the
Ministére de l'Enseignement Supérieur et de la Recherche and of CNRS, and in the Molecular Systematics section of
the Jodrell dista (Royal Botanic Gardens, Kew) with the support of a SYS-Resource grant and RBG Kew. Many
thanks to V. Savolainen (Royal Botanic Gardens, Kew) for his invaluable help with the a iie analysis. We thank
the tropical greenhouses team at the Arboretum de Chévreloup (MNHN, France), “Les Cédres” Botanic Gann (St.-
Jean Cap-Ferrat, France), and the Botanic Garden of Heidelberg (Ge many) rae authorizing hee rst author to sample
from their living collections for the DNA studies; Luciano 5 head of LME-CNRE Mads acca and Lanto,
who drove our vehicle throughout Madagascar

? Muséum National d'Histoire Naturelle, Dipin de Systématique et Evolution, Institut de Systématique, CNRS
(FR1541), 16 rue Buffon, 75005 Paris, France. haever@mnhn.fr; labat@mnhn.fr.

* Herbarium, Royal Botanic Gardens, Kew, Ric 2 Surrey, TW9 3AB, U.K. p. holimann@rhgkew., org. u

Missouri Botanical Garden, P.O. Box 299, St. Lo Моля 63166- 0299, U.S.A., and Département de T
lique et Evolution, Muséum National d’Histoire Naturelle, 16 rue Buffon, 75005, Pari ейная lowry@mobot.org.

aboratoire de Microbiologie de l'Environnement, Centre National de Rechere hu sur Environnement, Antana-
narivo 101, Madagascar. Imecnre@dts.mg.

ANN. Missouni Bor. GARD. 91: 247-259. 2004.

Annals of the
Missouri Botanical Garden

vide a basis for developing a revised taxonomy of
the ca. 80 species (ca. 120 if the infraspecific taxa
are included) present on the island (Haevermans,
2003). The spiny succulent Euphorbia, which com-
prise the Crown-of-Thorns (Euphorbia тїй Des
Moul.) and its relatives, have been referred to by a
variety of names in the past. Boissier (1862) estab-
lished Euphorbia sect. Diacanthium to accommo-
date the spiny members of the genus, including the
spine-shield-bearing species from Africa as well as
the Madagascan leafy spiny species. Many authors
have accepted this concept, with minor changes
concerning its rank and placement within the ge-
nus, including Bentham and Hooker (1880), who
recognized Diacanthium as a subsection within
e broadly defined section Figen uud

87) reassessed the status of Madagascan and Af-

Gilbert

rican Diacanthium, as well as some species previ-
ously included in subgenus Rhizanthium, which
was originally circumscribed to include all the geo-
phytic taxa from various parts of the paleotropics.
He placed all the Madagascan species of Diacan-
thium in a new subgenus Lacanthis (Raf.) Gil-
bert [based on Lacanthis Raf., Fl. Tell. 94 (1837),
type: L. splendens (Bojer) Raf.], which includes all
the spiny taxa (ca. 80 species) as well as about 10
geophytic species (e.g.. E. rubella from Ethiopia
and E. primulaefolia from Madagascar); the spine-
shield-bearing species of Euphorbia from Africa
and India (about 200—300 species) were restricted
to aptas Euphorbia (cf. Carter, 1982). Rauh
(1995, continued to refer to the

Madagascan spec ies as “Diacanthium” or the “E,

owever,

milii complex

Gilbert’s (1987) circumscription of Euphorbia
subg. Lacanthis provides a useful hypothesis
against which to assess the position of the succulent
species in Madagascar within the genus, and to
evaluate relationships among the species currently
assigned to the group. In this study we have used
two approaches to reconstruct a phylogeny based
on molec a sequence data from the ITS] + 5.85

rDNA region (hereafter referred to as the

ITS regic 80 Maximum Parsimony (MP) and Bayes-
ian a е (BI) coe eds k & Ronquist, 2001;
. Bayesian analysis has
recently been Be. in a variety of ways, e.g.,
paralogy in inferring organismal phylogenies (Mar-
tin & Burg, 2002), basal avian divergence (Braun
& Kimball, 2002), and human origin (Huelsenbeck
& Imennov, 2002).

uelsenbeck et al.,

MATERIALS AND METHODS
SAMPLING

The nrDNA regions ITSI, 5.88, and ITS2 were
sequenced for 30 taxa (Appendix 1); sequence data

for the remaining 20 taxa were made available by
V. Steinmann (Steinmann & Porter, 2002). Two out-
groups were chosen from tribe Euphorbieae, sub-
tribe Anthosteminae (a potentially new species of
Anthostema from Madagascar) and subtribe us
guillauminiinae (Calycopeplus casuarinoides L.
Sm. from Australia). Their appropriateness as out-
groups has been demonstrated by Steinmann and
Porter (2002)

The ingroup includes representative taxa of Eu-
phorbia subg. Lacanthis, as circumscribed by Gil-
bert (1987),
known to be closely allied (Steinmann & Porter,
2002),

Croizat and section Denisophorbia (Leandri) Cro-

plus a few Madagascan endemics
such as members of section Deuterocalli

izat, as well as E. emirnensis, an endemic member
(from Madagascar and the Comoros) of subgenus
Esula Pers. Two species were included as repre-
sentatives of subgenus Euphorbia, E. drupifera from
Africa and E. epiphylloides from India.

DNA SEQUENCING

Leaf fragments or young green shoots (for leafless
plants) were desiccated in the field with silica gel
for subsequent DNA extraction (Chase & Hills,
1991). Dried Euphorbia material was ground using
Mixer Mill MM 300™ with tungsten carbide
beads (from Qiagen Inc.), and the total DNA was
extracted with the Dneasy™ Plant kit (Qiagen Inc.)
following the manufacturers protocol (without liq-

A
—

uid nitrogen for grinding the plant material). Before
PCR, total DNA was purified a second time (to min-
imize РСК reaction inhibitions) with the Qia-
quick™ PCR Purification Kit (Qiagen Inc.).

The entire ITS region (ITSI + 5.85 + ITS2) was
amplified by PCR (28 cycles, 2 min. premelt at
94°C, 1 min. denaturation at 94°C, 1 min. anneal-
ing at 50°C, 3 min. extension at 72°C, 7 min. final
extension at 72°C) using two primers: ABIOIF (57-
ACG AAT TCA TGG TCC GGT GAA GTG TTC G-
3°) and ABIO2R (5-TAG AAT TCC CCG GTT CGC
TCG CCG TTA C-3’) from Sun et al. (1994). Three
percent DMSO (1M) was added to the reaction to
improve the results.

PCR products were purified with a Concert™
Rapid PCR Purification System, and then cycle-
sequenced with the same two primers, with dye ter-
minator and 3% DMSO (1M). Cycle sequencing re-
actions were purified by ethanol precipitation and
run on a PE 3777 automated gel sequencer (Ap-
plied Biosystem Inc.) following the manufacturer's

protocol.

Volume 91, Number 2
2004

Haevermans et al. 2
Madagascan Euphorbia Subgenus Lacanthis

SEQUENCE ALIGNMENT AND PHYLOGENETIC

ANALYSIS

Sequences were assembled and edited using Se-
quencher® 3 (Genecodes). The resulting matrix was
then aligned with the help of POY®, a program that
implements the direct optimization and fixed states
procedure described in Wheeler (1996, 1999). The
resulting matrix was also visually edited with the
help of BioEdit? (Hall, 1999).

For the MP and bootstrap resampling (Felsen-
stein, 1985), the insertion/deletion
events (indels) present in the aligned matrix were
coded following the method explained in Barriel
(1994), and automated using the software Barcod®
ver. 182, 02/09/1998. The coding method applied
by this software is based on the three following

rules: (1) an indel corresponds to a unique mutation

numerous

event, whatever the number of nucleotides implied,
so one indel is treated as equivalent to one char-
acter; (2) when many taxa share an indel, the cod-
ing system must consider it as a shared state; (3)
system must not add any evolutionary
steps. This results in the insertion in the matrix of
an “I” or "D" (for insertions and deletions), or of
7?" (to be interpreted here not as missing data, but
as uncertainty, which then could be subsequently

the coding

optimized).

The “barcoded” matrix was analyzed with
PAUP*4.10b for PC (Swofford, 1998) on an AMD
Athlon XP1400+ based computer with 256 Mb of

MP analysis was run as follows: heuristic
search with tree bisection-reconnection (TBR)
branch swapping method, random addition se-
quence, 1000 replicates, character state optimiza-
tion set on “accelerated (ACC-
TRAN), steepest descent not in effect. Bootstrap
resampling was performed as follows: parsimony
optimality criterion, 500 replicates with TBR swap-
ping algorithm and holding 10 trees per replicate.

e Bayesian Inference method (BI) used here
represents a Maximum Likelihood (ML)-type ap-
proach combined with confidence testing expressed

transformation”

in the form of posterior probabilities for the trees
obtained in the analyses (Huelsenbeck & Ronquist,
2001). The
and BI is that the latter provides posterior proba-
bilities for the hypotheses tested, not probabilities
of data given a hypothesis. The Bayesian analysis
was conducted using MrBayes 2.01 (Huelsenbeck
& Ronquist, 2001), on an aligned matrix without
gap coding, using the HKY85 nucleotide substitu-
1985), which allows

base frequencies to vary, as well as different sub-

fundamental distinction between ML

tion model (Hasegawa et al.,

stitution rates between transversions and transi-
tions.

The analysis of the data set was run using 10°
generations, which were performed on four Markov
chains with trees sampled every 100 generations
and with a uniform prior distribution (meme ngen
= 1000000 printfreq = 100 samplefreq = 10
nchains = 4/lset nst = 2 rates = equal). The Mar-
kov chain convergence occurred rapidly (before 1.5
х 10! er to ensure subse-
quent sampling of topologies the first 3000 trees (3
“burn-

generations), so in orde

Q' generations) were discarded as the °

of the process.

RESULTS
MAXIMUM PARSIMONY

Of 745 total characters, 290 were constant, 109
variable but parsimony uninformative, and 346 po-
tentially parsimony informative. The analysis yield-
ed 809 equally parsimonious cladograms each
1212 steps in length (CI = 0.5652, RI = 0.7142),
one of which is shown in Figure 1, with bootstrap
resampling values and nodes collapsing in the strict
consensus indicated by a dot. The ingroup is mono-
phyletic (BS = 100%). Euphorbia emirnensis, a
representative of subgenus Esula, branches first,
followed by E. pachysantha (a 5 of sect. De
isophorbia (Leandri) Croizat s.l., = 100%). The

st part of subgenus о. sensu Gilbert
(1987) branches next (BS = 96%); it comprises E.
brunellii and E. rubella, two species from mainland
Africa, which form a well supported clade (BS =
100%). The next branch (BS = 96%) comprises the
two sampled species of subgenus Euphorbia (BS =
100%), followed by the clade representing section
Deuterocalli (BS = 100%), which lies sister to the
Denisophorbia + Lacanthis s. str. clade and com-
prises Madagascan sub-aphyllous endemics. The
sister group relationship between section Deniso-
phorbia s. str. (which includes relatives of E. pyri-
folia, four of which are sampled here) and subgenus
Lacanthis s. str. is only moderately supported (BS
= 68%), and support is likewise limited for the
monophyly of subgenus Lacanthis s. str.

0%).

Although the branching pattern within Kuphor-
bia subg. Lacanthis is weakly supported, several
clearly defined clades can be identified (Fig. 1).
The first to branch (BS = 83%) comprises species
from the northern and eastern parts of Madagascar,
divided into two subclades: the first one (the .
tharanae clade, BS = 100%) contains E. capman-
ambatoensis and E. iharanae, and the second one

(the E. thuarsiana clade, BS = 65%) has four spe-

250 Annals of the
Missouri Botanical Garden

E. brachyphylla
— E E ны Е. gottlebei clade
“Г E ее
D E. croizatii E. croizatii clade
E. cremersii
ГТ Е. horombensis
69 Е. ankazobensis MN .
E. quartziticola E. didiereoides clade
d E. didiereoides
100 r7 E. annemarieae E. lobh РР
82 Е. lophogona | . lophogona clade
E. primulaefolia
100 ieri Ч
— a o i ا‎ E. perrieri clade мі
Е. paulianii u
_85| z9r E. milii B 2
90 E. milii А E. milii t
" 97 EE aff. beharensis var. guillemetii clade S
. beharensis я
— sr Е. parvicyathophora | E. tulearensis clade 2
| E. tulearensis С
Е. cylindrifolia р
ү — E. boissien | E. boissieri clade 2
E. viguieri
96 [- E. ankarensis
= E. millotii Е. апкагепзїз с\айе
60 Е. pachypodioides
61 E. robivelonae
2 Е. geroldii Е. thuarsiana clade
= E. thuarsiana
83 . bulbispina
68 |
— 00 Е. capmanambatoensis В
1 E. iharanae
E. capmanambatoensis A clade
E. iharanae
77[- E. elliotii
100) a E. hedyotoides section
E. boivinii Denisophorbia s.s.
E. mahabobokensis
% в1г— E. alluaudii ssp. oncoclada B
m 100 E. alluaudii ssp. oncoclada А | SeC ction
Lap E. cedrorum Deuterocalli
96 E. alluaudii
100[- E. epiphylloides | :
subgenus Euphorbia
100 —E drupi 9 р
100r- E. brunellii |
in L la subgenus Lacanthis 5.1.
E. pachysantha
E. emirnensis
= Calycopeplus casuarinoides

Anthostema sp. aff. madagascariense

Figure l. One of the 809 most parsimonious cladograms with a length of 1212 steps (CI = 0. — RI = 0.7142).
Bootstrap resampling values are given above the supported branches; nodes collapsing i in the strict consensus tree are
indicated by a dot. (Euphorbia emirnensis is in E. subg. Esula, E. pachysantha is in E. sect. De ds (Only BS
greater than 50% are given.

Volume 91, Number 2
2004

Haevermans et al. 2
Madagascan Euphorbia Subgenus Lacanthis

cies, one of which, the spiny E. bulbispina Rauh.
branches first, with three inermous species (L. ro-
and E.

forming a moderately supported subclade

bivelonae, E. geroldii, thuarsiana) then
82%). The next branch within subgenus Lacanthis
is the E. ankarensis clade, which comprises two
northern Madagascan species (E. ankarensis and E.
millotii; BS = 96%) that are sister (BS = 63%) to
E. pachypodioides, whose spines are borne on a po-
i 1947). The F.

unites the two distinctive monopodial species H.

darium (Boiteau, boissieri clade
boissieri (with inconspicuous erect cyathophylls)
and H. viguieri (with showy erect eyathophylls), al-
though bootstrap support is weak. This group is sis-
ter to a large clade (BS =
the spiny species of subgenus Lacanthis, as well as
the Madagascan geophytic taxa. This large group is
divided into two unequally supported subclades.
The first contains the succulent leafy geophytic
species E. cylindrifolia, which m before a
98%) con-

taining E. tulearensis and E. parv a (two

clade (the E. tulearensis clade,

other dwarf geophytes), and is sister to the E. milii
clade (BS —
(BS = 79%) and the closely related E. beharensis
and E. aff. beharensis var. guillemetii (BS = 97%).
The second subclade (BS = 82%), with 15 species,
contains the closely related E. perrieri (originally

= 90%), containing the spiny Z. milii

misspelled as “E. perieri”) and E. paulianii, form-
ing the E. perrieri clade (BS = 100%), which

branches basally to a large, poorly resolved clade

—

comprising the remainder of the species sample
from subgenus Lacanthis. Within this group, how-
ever, four subclades can be seen (Fig. 1), each com-
prising from two to four species.

BAYESIAN INFERENCES OF PHYLOGENY

The BI tree is given in Figure 2. The overall
topology is very similar to that of the MP tree (Fig.
1) but with better node support, and the clades de-
fined in the tree are strongly congruent with mor-
phology. All of the basal nodes have a probability
of 1.00 and the value for the sister group relation-
ship between Euphorbia sect. Denisophorbia s. str.
and subgenus Lacanthis s. str. is P = 0.91. The
monophyly of the Madagascan members of subge-
nus Lacanthis is likewise well supported (P —

0.99), and in contrast to the MP analysis, most of

the internal nodes are satisfactorily supported (P —
0.91 to 1.00). The subclade comprising six species
(from E. robivelonae to E. iharanae) is well sup-
ported (P = 1.00) and its internal structure is best
interpreted as a polytomy with three entities: the F.
tharanae clade (Р = 1.00), E. bulbispina, and the

85%) containing most of

E. thuarsiana clade (P = 1.00). The basal position
of E. us hypodioides within the E. ankarensis clade

F:

is well supported, and Æ. cylindrifolia
is s clearly sister (P = 0.97) to the lineage (P =
(Р =

. The position

1.00) comprising the E abba clade
1.00) + the E. milii lada (P=
of the E. perrieri clade is well m d (P — 1.00),
unlike in the MP analysis. The sister relationship
of the E. lophogona clade and the E. didiereoides
clade is well supported (Р = 0.98), and the latter
1.00), although res-
olution among the four species within the E. didi-

is clearly monophyletic (P —

ereoides clade is weak. The E. gottlebei clade is also
well supported (P — 0.97), as is the sister relation-
ship of E. mahafalensis and Е. croizatii (Р = 1.00).
For the geophytes, the positions of E. primulaefolia
and H. cremersii are doubtful as the branching pat-
terns are not supported, and in any case they do
not appear to be related to the other geophytic spe-

analysis, E. quartziticola,

cies included in the

which is clearly a member of the E. didiereoides

clade.

DISCUSSION

POLYPHYLY OF EUPHORBIA SUBG.
GILBERT

LACANTHIS SENSU

Gilbert’s (1987)
subg. Lacanthis encompassed spiny leafy plants

circumscription of Euphorbia
(such as E. milii). geophytes (e.g., the Madagascan
E. quartziticola and the Ethiopian E. rubella), and
trees (E.
Steinmann and Porter (2002) included a few mem-

sub-inermous rainforest thuarsiana).
bers of Euphorbia subg. Lacanthis in their study of
tribe Euphorbieae and showed that the Z. rubella
group from Africa was not directly related to the
Madagascan taxa of Lacanthis. Our results, based
on an expanded sample of species from Madagas-
car, with more geophytes, confirm this finding. Both
the MP and BI analyses clearly show that the Af-
rican species included by Gilbert (1987) in sub-
genus Lacanthis are not closely related to those
from Madagascar, but rather form a distinct clade
that occupies a more basal position within the trees

(Figs. 1, 2)

MONOPHYLY OF THE MADAGASCAN MEMBERS OF
EUPHORBIA SUBG. LACANTHIS

The results presented here strongly support the
interpretation that the members of Euphorbia subg.
Lacanthis in Madagascar form a well-defined clade.
Our expanded sample, comprising 33 of the esti-
mated 80 species in the group (Haevermans, 2003),
covers almost all of the morphological and geo-

252 Annals of the
Missouri Botanical Garden

E. brachyphylla
i E. gottlebei clade

E. croizatii clade

E. didiereoides clade

E. annemarieae
E. lophogona
E. primulaefolia
E E. perrieri
—E paulianii

| E. lophogona clade

| E. perrieri clade

E. milii A E. milii

E. aff. beharensis var. guillemettii | clade

E. beharens

E aaa
. tulearensis

| E. tulearensis clade

subgenus Lacanthis s.s.

10
mmm!
o
=
5
Q
3
©
5

117 8
Q > x

ankarensis
millotii
pachypodioides
robivelonae
geroldii
thuarsiana
bulbispin

ca 5 B
capmanambatoensis A
iharan

elliotii

hedyotoides ection
eke 5 5.5.

Е. ankarensis clade

E. thuarsiana clade

—

©
л
= Я
— — 2 o6
о
E с |

: iharanae
lade

1

boivi
Шз ssp. oncoclada B

alluaudii ssp. oncoclada A | section
cedrorum Deuterocalli
alluaudii
epiphylloides |
. arupi

SN

o
N

subgenus Euphorbia

IE E. brunellii | А
n .
L E rubella subgenus Lacanthis s

1
1
1
1
—— Calycopeplus casuarinoides
Anthostema sp. aff. madagascariense

Figure 2. Fifty percent majority rule consensus tree obti au ae m the. Bayesian analysis showing the posterior
probabilities for each of the clades. (Euphorbia emirnensis is in E. subg. Esula, E. и is in K. sect. Deniso-
phorbia.)

Volume 91, Number 2
2004

Haevermans et a 2
Madagascan Euphorbia Subgenus Lacanthis

graphic variation, leaving little doubt that the lin-
eage evolved in Madagascar from a single common
ancestor. It is therefore clear that subgenus Lacan-
this should be circumscribed more narrowly than
originally suggested by Gilbert (1987), and should
All the

Madagascan taxa assigned to the subgenus by Gil-

include only the species from Madagascar.

bert share a suite of gross cyathial features, where-
several as-
(4 +
2) and the pendulous habit of the female flower.

as the East African. species. differ

pects, most notably in the number of Jok

although these characters do not offer any insight

as to their affinities with the extra-Malagasy spe-

cies. Including only the Malagasy species. the
members of subgenus Lacanthis thus appear to

have the following morphological synapomorphies:
well-developed cyathophylls that are as long as or
longer than the cyathium, a consistently hermaph-
rodite cyathium with 5 equal glands, an erect fe-

male flower, and verrucose seeds.

POLYPHYLY OF EUPHORBIA SUBG. RHIZANTHIUM

As indicated above. the Old World geophytic
species of Euphorbia were long conceived as form-
ing a group of their own, subgenus Rhizanthium
Rhizanthium

Boiss.). regardless of their geographic distribution

(Boiss.) Wheeler (based on sect.

and anatomy/morphology. The validity of this het-
Bally
(1967), and Gilbert (1987) regarded it as a grade

rather than a clade, which prompted him to include

erogeneous group was first. questioned. by

some species previously assigned to subgenus Rhi-
B e D

zanthium within his newly established subgenus

Lacanthis, dispatching the remaining species to
other existing groups. Based on our sampling.

which includes eight geophytic species from Mad-
agascar, it is, however, evident that the Madagascan
taxa traditionally placed in subgenus Rhizanthium
do not form a monophyletic group. The geophytes
from Madagascar are scattered. along the clado-

gram, some forming a grade basal to the £. milii
clade, while others are nested within well-support-
ed clades that otherwise do not contain geophytes

T

(e.g... E. quartziticola is part of the E. didiereoides

-

clade. and H. cremersti is a member of the E. cro-

izatit clade). It is interesting to note that none of
the geophytes sampled here are members of the
basal clades within subgenus Lacanthis s. str. (i. E.

and H.

clades). Moreover, among the species that were nol

the E. iharanae, E. thuarsiana, ankarensts

included in our study, there is none likely to be a

member of or closely related to these basal clades.

Table 1. Classification of Madagascan spiny succulent
ists developed by Ursch and Leandri (1954).

А honey Boileau
oiteaui Leandri

E. ankarensis group

a oisit M" andri
millotii Ursch &
. boissieri E ill.

Leandri

pa pa fa P Eo

К. lophogona group

ta

euconeura Boiss.

=

. lophogona Lam.
лвбйштбе rii Boileau

аг E a Sw
Gr 63
RI.
I
кү. S
a N
8 S
24 еч.
>
=
Эч

=
د

E. milii group

r
CR] US UT
د‎
х х
сї
a =.
=
C$ `
оол
5
Б®
T
e
E
a
Ex

I
—

3 capuri mii Ursch & Leandri

Се

decaryt Guillaumin
delphinensis | ا‎ & Leandri
denisiana Guill: aumin

EO rani Ursch
iarantsoae Т rsch 1 сапап

yt

Leandri

Um US CN
R >
$4
: 8
~
=
E
©
=
X
=
=
ES
a
3
=
a
سر‎

ا

UCM UN UN
jeu aes
q ie iy
= 6 =
~ Ss -
a 8 2
—
2 88
(NN
SR ы
ORE К
S. ©
— `
SE m
cS =
3 QA &
SE
са D"
8 ty
Y —
an
& om @
= Ж
a —
=

quartziticola Leandri
razafinjohanii Ursch & Leandri
. tardieuana Leandri

Sm CM Cm ту Се

. Isimbazazae Leandri
К. ae
oup E. pachypodioides Boiteau
Я one.
biaculeata Den

group js
Е. ре xdilanthoides De nis

I. perrieri group Е. caput-aureum Denis
E. croizatii. Leandri
E. didiereoides Denis
H. guillauminiana Boite au
H. pauliani nit Ursch & Leandri
E. perrieri Drake

RELATIONSHIPS WITHIN EUPHORBIA SUBG.
SENSU STRICTO

LACANTHIS

Ursch and Leandri (1954) published the only
comprehensive review of the taxonomy of the suc-
culent spiny Madagascan Euphorbia, in which they
described several species and hybrids based on
plants of uncertain origins cultivated in the Pare de
Tsimbazaza (Antananarivo, Madagascar). A sum-
mary of their classification is given in Table 1. At
that time only a small number of Madagascan taxa
were known, and the recognition of many new spe-
cies since then has shown that the informal groups
established by Ursch and Leandri (1954) are un-
satisfactory. Rauh in particular named many spe-

cies from Madagascar, and attempted a synopsis of

254

Annals of the
MEE Botanical Garden

their classification in two popular books (Rauh,
1995, 1998)

Several authors (Croizat, 1965, 1967, 1972; Cre-
mers, 1984a, 1984b, 1989) have placed the Mad-
agascan species of Euphorbia in a series of informal
groups on the basis of their gross morphology, al-
though their
grades rather than clades. For example, some spe-

"groups" might in fact represent
cies are distinguished by monopodial growth, re-
ferred to by Cremers (1984a) as “Euphorbes mon-

LE]

ocaules," despite the fact that mature individuals
eventually exhibit some branching. Species exem-
plifying this cie form are E. boissieri, E. cap-
and E.
Some other taxa бе been assigned to the E. milii
complex (Rauh, 1995, 1998) and are typically rep-
resented by spiny species with showy cyathophylls.

manambatoensis, lophogona, viguleri.

THE EUPHORBIA IHARANAE AND E. THUARSIANA CLADES

Ursch and Leandri (1954) included Euphorbia
neohumbertii in their E. lophogona group, which
unites the monocaulous species and с и to
the expanded concept of Cremers (19 le
cladograms presented in Figures 1 and 2 di not,
however, support this interpretation, as the mono-
caulous species do not appear to form a clade.
Within subgenus Lacanthis s. str. (Figs. 1, 2), the
first clade to branch contains monocaulous relatives
of E. neohumbertii (1.e., E. capmanambatoensis and
E. iharanae) but is sister to the shrub to tree-like
inermous relatives of E. thuarsiana (F. tardieuana,

E. geroldii, and E. robivelonae). These inermous

species, initially placed by Ursch and Leandri
(1954) in their E. milii group, were subsequently
thought to belong to Denisophorbia (Leandri, 1957),
a finding that is not supported by our data.
Among the species possessing true spines, only
Euphorbia bulbispina was known to occur in the
northern part of Madagascar (Rauh, 1998). Its po-
sition in a clade containing E. iharanae and Е.
thuarsiana (which grow in the same geographical
area) has never been proposed before. Despite hav-
ing spines, E. bulbispina is neither a member of the
E. milii clade nor any of its sister clades, and it

possesses a distinct and unique combination of

characters (including an obvious hypopodium and
the distinctive shape of its spines and cyatho-
phylls), which in light of our molecular results
could be reinterpreted to set it clearly apart.

THE EUPHORBIA ANKARENSIS CLADE

A similar case is presented by Euphorbia pachy-
podioides, which was placed in a group of its own
by Ursch and Leandri (1954) and Rauh (1995). Our

cladograms (Figs. 1, 2) show that E. pachypodioides
(from northern Madagascar) branches basally to the
clade comprising E. ankarensis and E. millotii, two
species which also occur in the northern part of the
island. Euphorbia pachypodioides differs by its cy-
athophylls, which are distinct but erect like those
of members of the E. ankarensis group. The position
of E. millotii was questioned by Rauh (1995), who
pointed out the similarity of its stipules with those
of E. thuarsiana. However, plants of E. millotii oth-

1

erwise resemble E. ankarensis and its allies (E. her-

manschwartzüi, E. denisiana, E. alfredii, not includ-
ed in the cladogram). The molecular analysis shows
that А. millotii is not directly related to E. thuar-
siana, but rather belongs to the E. ankarensis clade.

THE EUPHORBIA BOISSIERI CLADE

Another pair of distinctive monocaulous species,
Euphorbia viguieri and E. boissieri, were included
in this study because their presumed affinities to
the other species of Euphorbia were highly specu-

ative. Euphorbia viguieri has individual, multi-
branched spines with a thick base (whereas the
stipular formations of E. boissieri are soft and fleshy,
branched combs), and it possesses incyathescences
(i. e., cyathia borne in a kind of synflorescence) very
similar to those of E. capmanambatoensis, with the
same large, showy, erect cyathophylls (whereas
those of E. boissieri are reduced and inconspicu-
ous). For this reason, Rauh (1995) considered E.
viguieri a member of his E. neohumbertii group

also containing E. capmanambatoensis and E. au-

—

reoviridiflora). This view is refuted by the molecular
analysis presented here, as E. boissieri and E. vi-
guieri are likely to be more related to each other,
forming their own group, than to the other groups
of species

habia boissieri is a poorly known species
that was until recently known only from a single
collection made in 1852 on the Ile Sainte-Marie,
off the east coast of Madagascar. It was long con-
sidered extinet because its habitat, a single forest
on the island, had supposedly been totally de-
stroyed. No other collections of E. boissieri were
made until it was rediscovered in 2001 in the west-
ern part of the Masoala Peninsula, extending the
distribution well to the north of the type locality
(Haevermans, 2003). The taxonomic position of H.
boissieri had long been doubtful because of its re-
duced, inconspicuous cyathophylls, a unique oc-
currence in subgenus Lacanthis. Ursch and Leandri

p

1954), basing their argumentation on its monocau-
lous habit, suggested that E. boissieri was closely
related to E. lophogona, but our molecular analyses

Volume 91, Number 2
2004

Haevermans et al. 255
Madagascan Euphorbia Subgenus Lacanthis

refute this, showing instead its relationship to E.
viguleri.

THE EUPHORBIA MILII AND E. TULEARENSIS CLADES

The spiny Madagascan euphorbs, often referred
to as the E. milii complex, are best represented by
the well-known E. milii and its varieties and hy-
brids. To date, however, no attempts have been
made to identify its closest relatives within subge-
nus Lacanthis. Our molecular data (Figs. 1, 2) in-
dicate that E. milii is closest to the succulent leafy,
shrubby, spiny E. beharensis and E. aff. beharensis
var. guillemettit (Е. milii has thin, soft leaves).

Sister to this group (Figs. 1, 2) are the various
geophytic species growing in southern Madagascar
(e.g.. E. tulearensis and E. parvicyathophora), which
have the same tvpe of succulent leaves with un-
dulate margins as E. beharensis and its varieties.
This interesting assemblage of dwarf geophytic spe-
cies [Ё. tulearensis, E. parvicyathophora, and E. cy-
lindrifolia (herein shown in Figs. 1, 2), but also E.
and E.

not included in the present study] has been regard-

francoisit, E. capsaintemariensis, decaryi,

ed as a group of uncertain affinities. Ursch and
Leandri (1954) included E. francoisii in their H.
ankarensis group, but this species shows distinct
cyathial and habit features that more likely unite it
with the dwarf geophytes from southern Madagas-
car. Croizat (1972) later established section Rhi-
zanthopsis, typified by E. francoisii, as a formal
name for Ursch and Leandri’s E. ankarensis group.
Rauh (1998) placed these species in a group of
their own (including E. ambovombensis, E. capsain-
temariensis, E. cylindrifolia, E. decaryi, E. franco-
isit, E. parvicythophora, and E. tulearensis). which
he linked to the spiny E. milii complex through E.
tulearensis and E. parvicyathophora based on their
spine-like stipular structures. Cremers (1984b) in-
cluded Rauh's species, along with E. primulaefolia
and E. moratii, in his broad concept of “geophytic
euphorbs,” equivalent to Boissier's section Rhizan-
thium.

As suggested by Rauh (1998), Euphorbia tulear-
ensis and H. parvicyathophora are closely related to
E. milii, and they form a clade sister to the E. milii/
E. beharensis clade. This informal group of small
succulent plants identified by Rauh is more likely
a grade basal to the E. milii alliance than a true
clade, as E. cylindrifolia branches basally in the E.
1, 2).
thought to be directly related to E. milii (Ursch &
Leandri, 1954; Rauh, 1998), and thus derived from

5

the same ancestors as E.

milii clade (Figs. The other spiny species

cylindrifolia (and rela-

tives), are more likely to form a distinct clade (Ta-
ble 1, Figs. 1, 2)

THE EUPHORBIA PERRIERI CLADE

Euphorbia paulianii and E. perrieri are very
closely related (Figs. 1, 2), but their affinities with
the other representatives of the genus were previ-
ously unknown. These two species are similar i

growth form and possess distinctive upright gcns
phylls surrounding the eyathium, sharing an overall
resemblance with those of E. pachypodioides (from
the north) and £. didiereoides (from the central
high-plateau). However, they differ from E. pachy-
podioides and E. didiereoides in the morphology of

The F.

group, as originally defined by Ursch and Leandri

their spines and incyathescences. perrieri
(1954) (Table 1), is too comprehensive and it would
be more appropriate to restrict the group to E. pau-
lianii and Е. perrieri only, so that it corresponds to
the H. perrieri clade indicated in Figures | and 2.
This is consistent. with the suggestion made by
Rauh (1995), and reflects the fact that these two
species are the only members of the subgenus to
possess campanulate cyathia with erect. cyatho-

phylls.

THE EUPHORBIA LOPHOGONA, E. DIDIEREOIDES, E.
CROIZATH, AND Е. GOTTLEBEI CLADES

Evaluation of the affinities of the remaining spe-
cies in the Lacanthis s. str. clade is more difficult
due to low support at a number of nodes (Figs. 1,
2). The prin: lophogona clade is well sup-
ported (BS —
ship between E. lophogona and annamarieae
pointed out initially by Rauh (1991). The E. didi-
> = 100%) contains high-plateau

100%), confirming the close relation-

ereoides clade (BS =
species with complex spine patterns (with the ex-
ception of E. quartziticola, for which the evolution
of its geophytic habit appears to have induced a
reduction of the stem and of the spine system). The
other clades within the terminal part of the MP and
BI trees (Figs. 1. 2) are less supported, making it
difficult to assess relationships with confidence.
Among these groups, there is, however, a ten-
dency for morphologically quite dissimilar species
occurring in the same geographic areas to form
clades. For example, the high-plateau species Eu-
phorbia didiereoides (spiny bush reaching 2.5 m

—
у

high), Е. quartziticola (geophytic species), E. an-
kazobensis and E. horombensis (spiny shrubs) form
a clade (albeit a moderately supported one) despite
their divergent habit and spine and leaf morphol-
ogies. Euphorbia didiereoides was previously placed

in the E. perrieri group (Ursch & Leandri. 1954)

256

Annals of the
Missouri Botanical Garden

because of its distinctive cyathial and stipular
spine structure, but Rauh (1995) correctly pointed
out that these features have "no evolutive value."
All the species found in the E. gottlebei, E. croiza-
tii, E. didiereoides, and E. lophogona clades have
complex spines, which are absent in E. perrieri and
E. paulianii, as well as in other groups such as the
E. milii clade.

GEOGRAPHIC DISTRIBUTION OF EUPHORBIA SUBG.
LACANTHIS

Several interesting patterns can be seen in the
geographic distribution of members of Euphorbia
subg. Lacanthis. The shrub to tree-like inermous
species, such as E. thuarsiana and E. geroldii, are
restricted to the northeast of Madagascar and do
not occur in the drier areas in the western and
southwestern parts of the island. Euphorbia robi-
velonae is a riparian species restricted to areas that
are flooded on a regular basis, near the northeastern
town of Sambava. The clades comprising species
with more or less complex spine-like stipular for-
mations, such as E. milii, E. didiereoides, and E.
lophogona, are distributed in the central and south-
ern part of the island. The few spiny species from
the north (Е. pachypodioides and Е. bulbispina,
which are restricted to Ankarana and Windsor Cas-
tle, respectively, in the far north) are not closely
related to the southern spiny species, contrary to
what was previously thought, but instead belong to
clades also restricted to the north.

The results of our analysis show that the basal
clades of Euphorbia subg. Lacanthis s. str. are com-
posed of taxa from the northeastern part of Mada-
gascar, whereas the derived spiny clades tend to
show a central and southern distribution. This sug-
gests a northern origin for the subgenus, with the
basal species having minute spiny stipular struc-
tures (e.g., as seen in E. geroldii). From these forms
other spiny taxa such as E. milii evolved, diversi-
fying throughout the rest of the island and becom-
ing well adapted to the very dry southern areas. No
natural occurrence of the subgenus, as recircum-
scribed here, has been recorded elsewhere, even
on the neighboring island groups such as the Mas-
carenes and Comoros. Euphorbia subg. Lacanthis is
therefore strictly endemic to Madagascar. Moreover,
if the trend toward recognizing subdivisions of Eu-
phorbia as distinct at the generic level is accepted
(see Gilbert, 1987), then the members of subgenus
Lacanthis would certainly qualify as a distinct ge-
nus.

CONCLUSIONS AND PERSPECTIVE

The circumscription and relationships of Eu-
phorbia subg. Lacanthis are far more complex than
thought previously, and the groups recognized by
earlier authors on the basis of gross morphology
appear for the most part not to comprise monophy-
letic assemblages. Instead, the results presented
here suggest that closely related species tend to
have similar eco-geographical distributions. The
features that have traditionally been used to define
groups among succulent euphorbs, such as mono-
cauly (Cremers, 1984a) and a geophytic habit (Cre-
mers, 1984b, 1989), are in fact the result of con-
vergences likely reflecting similar environmental
pressures. This abundance of convergence, occur-
ring not only in subgenus Lacanthis but throughout
Euphorbia as a whole, suggests that an attempt to
build a phylogeny based exclusively on morpholog-
ical characters is not likely to yield reliable results.
It will therefore be essential to pursue additional
molecular studies to address the tremendous taxo-
nomic problems posed by this huge genus.

e hypothesis of a northern Madagascan origin
of Euphorbia subg. Lacanthis s. str., as well as a
narrower circumscription of the group, should now
be tested by identifying and analyzing one or more
plastid or mitochondrial genes, and by including a
broader species sampling in order to produce a ro-
bust classification that reflects phylogenetic rela-

tionships.

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258 Annals of the
Missouri Botanical Garden

Appendix 1. Herbarium vouchers and GenBank accession numbers for taxa in this study. Novel GenBank accession
numbers submitted by TH are indicated by an asterisk (*); the remainder were made available by Victor Steinmann
(cf. Steinmann & Porter, 2002). For herbarium vouchers, “nat.” refers to the country of origin. BGH рш the
Heidelberg Botanic Garden. Epithet terminations were corrected (ICBN, 1999) to E. boivinii (from Boivin, Rec. 60C
ЩЫ), to E. paulianii (for the type collector M. R. Paulian, Art. 60.11, Rec. 60C.1), and to E. perrieri (rejecting “perieri”

as a typographic error under Art. 60

;enban
accession number

Taxon Origin and herbarium voucher
Anthostema sp. aff. ои ariense Baill. Madagascar, Miller et al. 8840 (MO) AF537583
Calycopeplus casuarinoides L. Cultivated (nat. Australia), Steinmann 1407 AF537580
(RSA)
md aff. beharensis var. guillemetii ris d (nat. Madagascar), Rauh 72744 AJ508970*
andri) W. Rauh (HEID)
W alluaudii Drake Madagascar, Haevermans 48 (P, TAN AJ508969*
Euphorbia alluaudii subsp. oncoclada Madagascar (Toliara), Haevermans 137 (P, AJ508968*
(Drake) Friedmann & Cremers, acces-
sion
Euphorbia alluaudii subsp. oncolada Madagascar (Fianarantsoa), Haevermans 25 AJ508967*
(Drake) Friedmann & Cremers, acces- T
sion
Euphorbia ankarensis Boiteau Cultivated (nat. Madagascar), Steinmann AF537462
1482 (RSA)
Euphorbia ankazobensis W. Rauh & Hof- Cultivated (nat. Madagascar), Rauh s.n. AF508966*
stütter ;H 140151 (HEID)
Euphorbia annamarieae W. Rauh Cultivated (nat. Madagascar), Rauh 7557 AJ508965*
(HEID)
Euphorbia beharensis Leandri Cultivated (nat. Madagascar), Rauh 72078 AJ508983*
Euphorbia boissieri Baill. Madagascar (Masoala), Labat 3355 (Р, AJ508963*
TAN, TEF)

Euphorbia boivinii Boiss. Maius ar r (Masoala), Haevermans 235 (P, AJ508962*
Euphorbia brachyphylla Denis Cultivated (nat. Madagascar), Rauh 74943b AJ508961 *
(HEID)

Euphorbia brunellii Chiov. apud Chiarugi iion (nat. east tropical Africa), Stein- AF537486

mann 1495 (RSA)
Euphorbia bulbispina W. Rauh Medie" (nat. Madagascar), Rauh 68664 AJ508960*
(HEID)
Euphorbia capmanambatoensis W. Rauh, Cultivated (nat. Madagascar), Rauh 74546 AJ508959*
accession A (HEID)
Euphorbia capmanambatoensis W. Rauh, Cultivated (nat. Madagascar), Steinmann AF537476
ccession В 1468 (RSA)
Euphorbia cedrorum W. Rauh & Hebding Madagascar (Toliara), Haevermans 81 (P. AJ508958*
TAN
Euphorbia cremersii W. Rauh & Razafin- Cultivated (nat. Madagascar), Haevermans AJ508957*
dratsira s.n. (P)
Euphorbia croizatii Leandri Cultivated (nat. Madagascar), Rauh 72182 AJ508956*
(HEID)
Euphorbia cylindrifolia Marnier-Lapostolle Madagascar, Haevermans 68 (Р, TAN) AJ508955*
W. Rauh
Euphorbia didiereoides Denis ex Leandri Madagascar, Haevermans 54 (P, TAN) AJ508954*
Euphorbia drupifera Thonn. Cultivated (nat. Africa), Steinmann 1488 AF537480
(RSA)

Euphorbia elliotii Leandri Madagascar, Dorr et al. 3985 (MO) AF537478
Euphorbia emirnensis Baker Madagascar (Ankaratra), Haevermans 95 (Р, АЈ508964*
ГА №)

Euphorbia epiphylloides Kurz Cultivated (nat. Andaman Islands), Stein- AF537484

SA)

mann 1459

3.

Volume 91, Number 2
2004

Haevermans е

2
Madagascan et Subgenus Lacanthis

Appendix J. Continued.

Taxon

Origin and herbarium voucher

GenBank

accession number

Euphorbia geroldii W. Rauh

Euphorbia gottlebei W. Rauh

Euphorbia hedyotoides N. E. Br.

Euphorbia horombensis Ursch & Leandri

Euphorbia iharanae W. Rauh

Euphorbia lophogona var. tenuicaulis W.
auh

Euphorbia mahabobokensis W. Rauh

Euphorbia mahafalensis Denis
Euphorbia milii Des Moul., accession A

Euphorbia milii Des Moul., accession B
Euphorbia millotii Ursch & Leandri
Euphorbia pachypodioides Boiteau
Euphorbia pachysantha Baill.
Euphorbia parvicyathophora W. Rauh
Euphorbia paulianii Ursch & Leandri
Euphorbia perrieri Drake

Euphorbia primulaefolia Baker
Euphorbia quartziticola Leandri
Euphorbia robivelonae W. Rauh
Euphorbia rossii W. Rauh & Buchloh
Euphorbia rubella Pax ex Engl.
Euphorbia thuarsiana Baill.

Euphorbia tulearensis (W. Rauh) W. Rauh

Euphorbia viguieri Denis

Cultivated (nat. Madagascar), Steinmann
1467 (RSA)

Cultivated (nat. Madagascar), Steinmann
1471 (RSA)

err (nat. Madagascar), Steinmann
472-A (RSA)
C bd ated (nat. Madagascar), Rauh 73701
(HEID)

Cultivated (nat. Madagascar), Steinmann
58 (RSA)
Eulbvated (nat. Madagascar), Rauh 74322/

El
Cultivated (nat. Madagascar). Steinmann
1450 (RSA)
Madagascar, Haevermans 60 (P, TAN)
Madagascar (Vatovavy), Haevermans 40
(MO, P, TAN
Cultivated (nat. Madagascar), Steinmann
476 (RSA)
ns (nat. Madagascar), Steinmann
7 (RSA)
B (nat. Madagascar), Rauh 22871
(HEID)
Cultivated (nat. Madagascar), Rauh 73350
(HEID, P)
Cultivated (nat. Madagascar), Rauh 74690
(HEID)
Cultivated (nat. Madagascar), Rauh 73266b
(HEID)

Cultivated (nat. Madagascar), Steinmann
1483 (RSA)

Cultivated (nat. Madagascar), Steinmann
184 (RSA)

Madagascar (Itremo), Haevermans 6 (MO,
Р, TAN

Cultivated (nat. Madagascar), Rauh 73927
(HEID)

urne (nat. Madagascar), Steinmann

€ Bowie (nat. east tropical Africa). Stein-
mann 1464 (RSA)
— ‘ar, Leeuwenberg & Ranaivojaona

1585 (K
Cultivated (nat. Madagascar), Rauh 68552
(HEID

Cultivated (nat. Madagascar), Rauh s.n.
BGH 142199

AF537475

AF537459

AF537460

AJ508971*

AF537477

AJ508972*

AF537522

AJ508973 *
AJ508974*

AF537461
AF537463
AJ508975*
AJ508976*
AJ508977*
AJ508978*
AF537463
AF537466
AJ508979*
AJ508980*
AF537465
AF537487
AF537474
AJ508981 *

AJ508982*

HOOGLANDIA, A NEWLY
DISCOVERED GENUS OF
CUNONIACEAE FROM NEW
CALEDONIA!

Gordon McPherson?
Porter P. Lowry IP?

and

ABSTRACT

Hooglandia McPherson & Lowry (Cunoniaceae) is described from New Caledonia and recognized as distinct from
other Cunoniaceae on the basis of its unique unicarpellate (or pe rhaps pseudomonomerous) gynoecium, and the com-

bination of dioecy and drupaceous fruit, inter

Critically Endanger
Эме

vords:

alia. The single species, H. ignambiensis, known only from primary rain
forest on the upper slopes of Mt. Ignambi in northeastern New Caledonia, is assigned a provisional threat status of
ed.

conservation, Cunoniaceae, Hooglandia, New Caledonia.

RÉSUMÉ

Desc троп йе Mii niri McPherson & Lowry, nouveau genre de Cunoniaceae de Nou
mbres de la famille par un gynécée unicarpe 11е (év омео pseudomonomere) et, inter bn

1 forét primaire sons humide des pentes supérieures du M

d'espèce en Danger Critique lui est provisoirement attribué.

autres caracteres: dioicie et fruit « т é. Lunique

velle-Calédonie se distin-

зрёсе, Н. ignambiensis, n'est connue que de

t. Ignambi, au eae est de la Nouvelle-Calédonie; 5 statut

New Caledonia is widely recognized for its ex-
ceptional botanical diversity, with an estimated
seed-plant flora of just over 3000 species, nearly
77% of which are endemic (Lowry, 1998; Jaffré et
al., 2001; Morat et al., 2001), qualifying it as a
global biodiversity hotspot (Myers et al., 2000). The
flora is known for its numerous endemic gymno-
sperms and representatives of many primitive an-
giosperm families, including the remarkable genus
Amborella Baill. (see Soltis et al., 2000; Thien et
al., 2003; and references therein).

Recently, while collecting on Mt. Ignambi in the
northeast of the island, we encountered first a fe-
male and then a male individual of a distinctive
tree species, one that matched nothing in our ex-
perience. At the time we were unable to place the
specimens in any family, despite the fact that we
had abundant flowering and fruiting material

hand. Subsequent studies in the herbarium, search-
es of the literature, and discussions with colleagues
confirmed our initial impression that our two col-
lections did, in fact, represent an unusual new el-
ement of the flora.

Conspicuous features of the new plant—includ-
dentate, stipulate

ing its opposite, compound,

leaves; tetramerous, unisexual flowers; imbricate
sepals; lack of a corolla; biseriate stamens; disk
adnate to the ovary; unicarpellate (or perhaps pseu-
domonomerous) gynoecium; and drupaceous, bilat-
erally symmetrical, one-seeded fruit—suggested, in
various combinations, members of the Oxalidales
(such as the Cunoniaceae or Brunelliaceae) and the
Sapindales (such as the Simaroubaceae, Anacar-
diaceae, Burseraceae, or Sapindaceae). However, it
proved impossible to refer the new taxon to any of
the currently recognized genera in these families.

' The authors thank Т. Le Borgne and R.
Economique, Province Nord,
Direction des Ressources Naturelles, Province Sud,
was funded by a grant from the John D. and Catherine T.
= botanical data to conservation idea in New €

NA sample, to Helen Brinon and Pe

for logistical Nippon and permission to conduct inventory work on Mt. Igni
for access to «

Caledoni
ter Stevens for he Apful « comments on the райы. affinities of the new taxon, to

Pouytiela for assistance in the field; the Direction de Développement

ambi; and the
drying facilities and for other courtesies. Fieldwork
Mac Arthur Foundation for кше entitled “Application

| to Patr for analyzing the

Ne are gratefu Sweeney

и Keating for careful examination of the pollen and endosperm, and to Yevonn Wilson-Ramsey for preparing the

fine illustration

? Missouri Botanic ‘al Garden, Р.О. Box 299, St. Louis. Missouri 63166-0299, U.S.A. gordon.mcpherson@mobot.org;

pete.lowry@mobot.org.

Departement de Systématique et Evolution, Phanérogamie, Muséum National d'Histoire Naturelle, 16 rue Buffon,

75005 Paris, France

ANN. Missouni Bor.

GARD. 91: 260-265. 2004.

Volume 91, Number 2
2004

McPherson & Lowry
Hooglandia from New Caledonia

We were able to place our material only after an
analysis of molecular sequence data (Sweeney et
al.. 2004), which clearly showed that the species
belongs within the Cunoniaceae. There it comprises
the morphologically well-marked new genus that we
describe here. Its closest relative may prove to be
Aistopetalum Schltr., a genus of two species endem-
ic to New Guinea, which resembles our new genus

ts large, paniculate inflorescence, apetalous

in
flowers in which the disk is adnate to the ovary,
and indehiscent fruit.

Hooglandia McPherson & Lowry, gen. nov. TYPE:
Hooglandia ignambiensis McPherson & Lowry.

Ge enus novum, quoad folia opposita иаа ане sti-
culatas, flores te-

fructu drupaceo monospermo divergens et insuper petalis

nullis, disco ovarium adnato insolitum.

Hooglandia shares a number of features with
many of the 26 other genera of the family (Bradford
& Barnes, 2001: 2004), including

opposite, imparipinnately compound leaves, inter-

Bradford et al..

petiolar stipules, paniculate inflorescences, tetram-
erous flowers, a diplostemonous androecium, an in-
trastaminal disk, and a superior ovary. However. it
is unique among Cunoniaceae in combining a un-
icarpellate (vs. 2(3—5)-carpellate) gynoecium and a
bilaterally symmetrical, drupaceous fruit (vs. typi-
cally capsules or follicles, or occasionally (in Dav-
Don, and Aisto-
As well.

most Cunoniaceae are hermaphroditic (22 genera)

idsonia F. Muell., Schizomeria D.
petalum) radially symmetrical drupes).

and have petaliferous flowers (15 genera) with disks
(Bradford et
al., 2004), whereas Hooglandia uniquely combines

free from the ovary wall (20 genera)

dioecy. a condition it shares with Pancheria

Brongn. & Gris, Spiraeanthemum A. Gray, Vesse-
lowskya Pamp., and some Weinmannia lL. spp.. with
apetalous flowers in which the disk is adnate to the
ovary. The phylogenetic implications of the distinc-
tive characters exhibited by Hooglandia are dis-

cussed by Sweeney et al. (2004).
The new genus joins 104 other seed-plant genera
New Caledonia (Jaffré et al., 2001),

bringing the level of generic endemism to 15%.

endemic

Etymology. The genus is named in honor of
Ruurd Dirk Hoogland (1922-1994). who devoted
much of his career to the study of the Cunoniaceae
and Dilleniaceae while serving as a member of the
CSIRO New Guinea Group and later at the Austra-
lian National University, and then after his retire-

ment at the Muséum National d'Histoire Naturelle
1995). Ru Hoogland was an
excellent collector and an expert on the floras of

Norfolk Island,

in Paris (see Morat,
New Guinea, and Lord Howe lIs-
land.

Hooglandia ignambiensis McPherson & Lowry,

sp. nov. TYPE: New Caledonia. Province

Nord: Mt. Ignambi, SW of Tehambouenne,
20°27'35"S, 164%35'41"E, 1150 m, 4 May
2002. P. P. Lowry Il, G. McPherson, T. Le

Borgne & К. Pouytiela 5767 (holotype, P: iso-
types, CANB, MO [2 sheets], NOU). Fig-

ure l.

Arbor dioica, 6-8 m alta. € novelli pubescentes

duae 'entes; internodia cava. Folie ror op-
37 em longa: foliola (1117-19 op-

10.8 х

posita decussata 26—
posita chartacea oblonga vel subobovata (5. Ari

(2—)2.5-3.3 cm; hamis matura fere glabra. basi obtusa,
margine integra vel sparsim dentata, apice. acuminata,
nervis utroque costae latere 1 ri 4(—16); petioluli quia m

longi pubescentes; petioli 6.5—9.5 em longi, 2—3.5 mm

diametro; stipulae interpe 55 s lineares 8-10 mm lon-

bescentes, unusquisque axibus p iis 3 ascendentibus
5—1.5 em, in plan-
lis masculis ad 8 cm longis; ES ‘eae triangulatae. 1.5—
mm longae; cymulae flores 4—6 gere ies s; > brac teolae 0.8—
2 mm longae caducae; nadeli 0.3-1.5 mm longi arti-
culati, in parte inferiore pubescentes, in eon superiore

vel recurvatis, in plantis femineis (1—)1.

glabri. Flores masculi: sepala 4 discreta alba imbricata
2.5—3.5 mm longa, 2.5—3 mm lata, subincrassata, extus
glabra, intus villosa, ciliata; petala nulla: stamina 9(—9)
ой, anthesi 4 mm longa, filamenta 3 mm longa subcom-
planata, antherae 1 mm longae polliniferae dorsifixae ver-
satiles biloculatae dehiscentia longitudinali latrorsa; dis-
cus intrastaminalis basim
pistillodium (cum stylo

a vestigiales; stigma minuta. Flores feminei: pe 0
ut in ibas masculis; staminodia 8(—9) sub anthe
1.5 mm longa, antherae 0.5-0.75

г

mm longae quasi non
polliniferae: discus ini basim ovarii adnatus
arpello unico, ovarium
mm altum,

annularis; ерт ium ca superum

mm latum, unilo-

viride :

. аай энер quadratum аши, stylus et umbo
apicales, stylus albus linearis adpressus geniculatus, ca.
l mm longus, apex stigmaticus ene atus; ovula 2, api-

calia, anatropa. Fructus axillaris infra е in
axibus 3.66 ст longis, Pro pop quasi obovatus vel
ив us, complanatus, 3.0—4.2 «

tus, 0.5 c
mm diametro, exocarpium carnosur
tenuis, иктин rmium r aceum,

m longus, 2—2.2 em la-
roste iat at umbons ca. 5-6
lh

т Crassus, apic e

Semen unicum, testa
b ula recta, ca. 5 mn
. 18 mm e ca. 11 mm latae.

ı longa, cotyledones complanatae
virides, ¢

Dioecious. unarmed, sparsely branched, odorless
trees ca. 6-8 m tall. Twigs densely pubescent with
short, subappressed trichomes when young. gla-

brescent, with scattered lenticels, lacking evident

exudates: leaf scars cordiform, 5—6(—10) mm long.

262 Annals of the
Missouri Botanical Garden

Figure 1. Hooglandia ignambiensis McPherson & Lowry. —A. Flowering twig of female material. —B. Abaxial
view of a lateral leaflet. —C. Young female flower. —D. Female flower at anthesis, one sepal removed. —E. Male
flower at anthesis, one sepal removed. —F. Fruit. (A, B, C, D, and F based on Lowry et al. 5767, MO; E based on
Lowry et al. 5770, MO.)

Volume 91, Number 2
2004

McPherson & Lowry
Hooglandia from New Caledonia

0-7 mm wide; internodes hollow. Leaves imparipin-
nately compound, opposite, decussate, 26-37 cm
long at maturity; leaflets (11 to)17 to 19, opposite,
dark green and shiny above, paler beneath, char-
taceous, oblong to weakly obovate, (5.5-)6-10.8 X
(2-)2.5-3.3 cm, the lower (or 2) pairs smaller and
often elliptic; occasionally caducous; blade gla-
brous at maturity except for sparse, short, subap-
pressed hairs on the midvein beneath, the imma-
ture leaves sparsely short-subappressed pubescent
on both surfaces, more densely so along the midrib:
base obtuse, oblique in the lateral leaflets, margins
minutely thickened beneath, entire or occasionally
with | to 3(to rarely 7) very slender, fragile teeth
per side, these usually terminating secondary vein-
lets in the basal third of the blade, or sometimes
located instead near the apex, each tooth up to 1
mm long, the slender portion caducous and some-
times leaving behind a small, mucronate remnant;
apex acuminate, tapering to a short mucro ca. 1
mm long, venation brochidodromous or semicras-
pedodromous with 11 to 14(to 16) pairs of opposite
to subopposite secondary veins; domatia absent;
petiolules 4-6 mm long, tinged reddish purple (in
fresh material), short-subappressed pubescent,
channeled above; rachis tinged reddish purple,
with moderate to dense short, subappressed hairs:
petioles 6.5-9.5 cm long, 2-3.5 mm diam., ex-
panded somewhat at the base, flattened in dry ma-
terial; stipels absent; stipules interpetiolar, linear.

8-10
nearly to the base or the two halves completely free

subterete, mm long, occasionally divided
from one another and separated by up to 3 mm.
densely short-subappressed pubescent, caducous,
leaving a small oblate scar ca. 1.5-3 mm wide:
colleters absent. Inflorescences axillary, flowering
sub-synchronous, the terminal flowers opening only
slightly before the more basal ones, paniculate,
short-subappressed pubescent throughout, borne in
the axils of the upper 3 to 7 pairs of leaves, the
short basal peduncle (0—)1—5(—б) mm long and
bearing 3 ascending to recurved primary axes
(1-)1.5-4.5 cm long in female plants, to 8 em long
(1)2 to 6, subop-

posite, the lowermost sometimes abortive and leav-

in male plants, secondary axes

ing an evident scar, each subtended by a caducous,
narrowly triangular bract ca. 1.5—4 mm long, ter-
minating in a 4- to 6-flowered cymule, the lower-
most secondary axes also bearing | or 2 lateral cy-
mules (tertiary axes), flowers subtended by a
straight, spreading, narrowly triangular bracteole
ca. 0.8-2 mm long, caducous prior to anthesis,
leaving an evident scar; pedicels 0.3-1.5 mm long.
jointed at or below the midpoint, the proximal por-

tion pubescent, the distal portion glabrous. Male

flowers: sepals 4, distinct, white, imbricate in bud.
2.5-3.5 mm long, 2.5-3 mm wide, rather thick,
spreading at anthesis, glabrous abaxially, villose
adaxially, ciliate: petals absent; stamens 8(—9), sub-
equal, 4 mm long at anthesis and slightly exserted
beyond the sepals; filaments 3 mm long, somewhat
flattened; anthers 1 mm long, polleniferous. dorsi-
fixed above the basal lobes, versatile, bilocular, de-
hiscence longitudinal and latrorse: pollen spheroi-
dal, 13-16 рт diam., tricolporate, surface visibly
psilate, slightly irregular; disk intrastaminal, adnate
to base of the pistillode, annular, ca. 1.5 mm diam.,
slightly lobed around the bases of the filaments;
pistillode conical, ca. 1.5 mm high including the
erect style/stigma (1 mm long): locule and ovules
vestigial; stigmatic portion of style/stigma minute.
apparently unreceptive. Female flowers: sepals 4(5).
distinct, white, in bud the 2 outer imbricate over
the 2 inner, 2.5-3 mm long, 2.5—3 mm wide, rather
thick, somewhat spreading, glabrous abaxially, vil-
lose adaxially, ciliate; petals absent; staminodes 8(—
9). 1-1.5 mm long at anthesis, anthers 0.5-0.75
mm long, not or only slightly polleniferous, the pol-
len grains few, of various sizes, rarely containing
cytoplasm; disk intrastaminodial, adnate to the base
of the ovary, annular, lobed (sometimes deeply so)
around the bases of the staminodes: gynoecium bi-
laterally symmetrical (excepting the bent style):
ovary superior, green, somewhat flattened, | mm
long. 1 mm wide on the wider face, roughly square
in outline, glabrous, unilocular. the style/stigma
arising from one distal corner and a faintly bilobed
hump occupying the other distal corner, ovules 2,
apical, anatropous, both attached at one end of an
elongate, shallow trough. micropyle epitropous:
stvle/stigma white, ca. 1 mm long, linear but crook-
ed. not held erect, typically basally appressed to
top of ovary and bent about mid-length through 90—
180 degrees, the apparently stigmatic portion elon-
gate. Infructescences borne in axils of the 2 or 3
pairs of leaves or leaf scars just below the inflores-
cences, each with 1 to 3 primary axes 3.6-6 cm
long and bearing one or two fruit; fruit drupaceous,
light green (in nearly mature fresh material), asym-
metrically obovate to elliptic in outline, flattened
and thus bilaterally symmetrical overall, 3.84.2
cm long. 2-2.2 cm wide. 0.5

rowly acute, slightly beaked apex ca.

cm thick, with a nar-
З mm long
and a rounded distal boss ca. 5—6 mm diam., exo-
carp fleshy, endocarp hard; seed one, the other
ovule aborting; testa thin; endosperm starchy, the
grains spheroidal, (5-)7(-9) jum diam., oil not de-
tected; radicle straight, ca. 5 mm long: cotyledons

flat, green, ca. 18 mm long, ca. 11 mm wide.

Annals of the
Missouri Botanical Garden

Paratypes. NEW CALEDONIA. Province Noro
Mt. Ignambi, SW of Te or 20°27’ 35°,
„ 1150 m, 4 May 2002, P. P. Lowry II. G.
McPherson, T. Le Borgne & R. unida 5770 (CANB, G,
MO, NOU, P).

Although the new species is here interpreted as
unicarpellate, and thus unique within the family in
this feature, a remnant of a second carpel may be
present in the form of the astylous hump visible in
both the female flower and the fruit (Fig. 1). How-
ever, dissections of the ovary revealed no further
evidence that more than one carpel is involved. It
may also be worth noting that, although Cronquist
(1981) stated that the endosperm in the family is
oily or absent, Dickison (1984), Takhtajan (1997),
Fortune Hopkins and Hoogland (2002), and Brad-
ford et al. (2004) describe it as starchy, as it is in
Hooglandia.

Hooglandia ignambiensis is known only from
dense, primary rain forest on the upper slopes of
Mt. Ignambi in northeastern New Caledonia. The
area is part of the Mt. Panié massif, which extends
ca. 50 km from north of Mt. Mandjélia southeast to
Mt. Panié.
climates in New Caledonia, with recorded annual

The massif has one of the most humid

precipitation levels reaching 4000 mm (Section
d'Hydrologie de PORSTOM & Service Territorial de
la Métérologie, 1981), although rainfall on the up-
per slopes is certainly even higher (Lowry, 1998).
The Mt. Panié massif is characterized by the pres-
ence of micaschist and related metamorphic rock
types, in contrast to adjacent areas, which are
largely dominated by soils derived from other sub-
strates, including the distinctive ultramafic rocks
that cover large portions of New Caledonia (Paris,
1981).
The Mt.

mism, with numerous species recorded only from

Panié massif is a center of local ende-

the comparatively well-collected eastern side of Mt.
Panié, and many others restricted to one or a few
localities in northeastern New Caledonia. The palm
flora of the area is particularly diverse, with 10 spe-
cies endemic to the massif (Hodel & Pintaud,
1998). This led Pintaud et al. (2001) to recognize
the Mt. Panié massif as one of five phytogeographic
regions within New Caledonia based on the distri-
bution of palm species. Few plant taxa appear to
have been previously known only from Mt. Ignambi,
but an endemic new species of gecko was recently
described from the peak (Bauer et al., 2000).
Conservation Using the data available
and applying the IUCN Red Data criteria (IUCN,
2001), we assign Hooglandia ignambiensis a pro-
visional threat status of Critically Endangered (CR
D) because only two mature individuals are known

status.

|

Adansonia,
——., T. Jaf

to exist. The area in which the plant grows, how-
ever, does not appear to be under any immediate
threat. The single known population occurs well
within a sizeable area of pristine forest, where it is
protected from the fires that frequently burn in the
surrounding secondary grasslands. Although local
inhabitants occasionally hunt in the area, we saw
no signs suggesting they exploit forest products,
and other than the presence of a trail, a long-aban-
doned road, and a very small clearing on the sum-
mit, there was little evidence of human disturbance
within the forested area.

A PDF version of this paper, including color im-
ages of Hooglandia ignambiensis, is available at:
http://www.mobot.org/ OT/Research/
newcaledonia/hooglandia.pdf.

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new high- duum Bavayia (Reptilia: 1 8 tylidae)
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Bradford, J. C. & R. W. Barnes. 2001. Phylogenetics and
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a
.H. 3 Hopkins & R. W. Barnes. 2004.
Rig ik Pp. 91-111 in К. Kubitzki (editor), The

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Cronquist, A. 1981. An Integrated System of Classifica-
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Missouri

PHYLOGENETIC POSITION
OF THE NEW CALEDONIAN
ENDEMIC GENUS
HOOGLANDIA
(CUNONIACEAE) AS
DETERMINED BY MAXIMUM
PARSIMONY ANALYSIS OF
CHLOROPLAST DNA!

Patrick W. Sweeney,?? Jason С.
Bradford. and Porter P. Lowry IPS

ABSTRACT

To determine the phy logenetic m of a newly discovered New Caledonian E. Hooglandia McPherson &
we

Lowry, maximum 5 analys

rbcL and trnL-F data sets. A
F chloroplast data sets using a
‘ular dat

Key w ede

performed using molecular sequence dat
n initia 1 ын using an rbcL
edie a position ы Hooglandia within Cunoniaceae, a relationship further confir
a more focused sample of taxa from Oxalidales. The position of Hooglandia i in Cunoniaceae
is d by its possessing interpetiolar stipules and starchy endosperm. This paper provic

ooglandia and existing
data set with a broad ics of flowering xy о
med by analyses of rbcL rnL-

s a rare example келу

were used to guide the familial placement of a newly discovered plant genus concomitant with its

Cunoniaceae, DNA taxonomy, Hooglandia, molecular systematics, New Caledonia.

a companion paper, McPherson and Lowry
(2004, this issue) describe Hooglandia as a new
genus of Cunoniaceae from Mt. Ignambi in north-
eastern New Caledonia. When material of this new
taxon was first collected, it clearly represented a
new species and was regarded as possibly the first
material of a new genus or family. However, deter-
mining the affinities of the new plant proved prob-
lematic, as it had morphological features common
to members of both Oxalidales and Sapindales but
did not have a combination of features character-
istic of any of the families or genera within these
orders (McPherson & Lowry, 2004). To aid in the
taxonomic placement of Hooglandia, the first au-
thor conducted molecular phylogenetic analyses to

investigate the phylogenetic position of the newly
discovered taxon. While the impacts of molecular
phylogenetic techniques on plant systematics have
been substantial (e.g., Chase et al., 2000; Crawford,
2000; Stevens, 2000), their integrated use in the
placement of newly discovered taxa has not been a
common practice among plant systematists (but see
Garnock-Jones et al., 1996). Here we present the
results of a nested series of molecular phylogenetic
analyses using sequence data from two chloroplast
regions (rbcL and trnL-F) that proved essential for
determining the relationship of Hooglandia and as-
sessing its placement among the currently recog-
nized flowering plant families (McPherson & Lowry,
2004)

' The authors thank Peter Stevens and an anonymous reviewer for comments on the ге ript and Andrew Doust
l te

for assistance in evaluating the combinability of the data sets. We are

Economique, Province Nord, for logistical support

of this study was supported by the E. Desmond Lee La

and permission to conduc
was funded by a grant from the John D. and E Bep ud и МасАг

tory of Molec

also dis to the
entory sein
thur Foundation (to

direc 1 0 de Développement
gnambi. Fieldwork

St. Louis. We also thank Richard Keating of the Missouri В al Ca for help in evaluating stomatal anatomy in

—

Missouri Botanical ар

3 University of Misso

U.S.A.
t University «

California 95616

P.O. Box 299, Saint Le

pwsd POA lentil. umsl.e
of 8 9 0
S.A.

ouis, Missouri 63166-0299, U.S.A.
ri-Saint Fach Biology Department, 8001 Natural Bridge Road, Saint Louis, Missouri 63121,

nia а! Davis, Department of Environmental Science and Policy, One Shields Avenue, Davis,

Departement + r Systématique et Evolution, Phanérogamie, Muséum National d'Histoire Naturelle, 16 rue Buffon,

75005 Paris, Franc

ANN. Missouni Bor.

GARD. 91: 266-274. 2004.

Volume 91, Number 2
2004

Sweeney et al. 267
Hooglandia DNA Analysis

MATERIALS AND METHODS
CHOICE OF MARKERS

Two molecular markers from the chloroplast ge-
nome (rbcL and trnL-F) were selected for the phy-
logenetic analysis of Hooglandia. They were chosen
for three main reasons: (1) many sequences from
these regions were readily available in internet da-
(2) their taxonomic

tabases: representation. was

broad; and (3) the level of sequence variation
seemed appropriate for assessing the phylogenetic
placement of the new entity at the ordinal and fa-
milial levels. An initial analysis was performed to
place Hooglandia within the angiosperms using the
(1993),

proven useful in resolving relationships among the

rbcL data set of Chase et al. which has
major groups of flowering plants. Once the first
analysis indicated that. Hooglandia was related to
members of Oxalidales (sensu APG, 2003), and in
particular to Cunoniaceae, the trnL-F and rbcL data
sels of Bradford and Barnes (2001) were then used
to evaluate the likely position of Hooglandia within
the order. The Bradford and Barnes (2001) data sets
included representative genera from across Oxali-
dales as well as a nearly comprehensive sampling
of genera from Cunoniaceae. All of the data sets
study are available in

1994—2003,

utilized in the present
TreeBASE (TreeBASE ©

treebase.org).

WWW.

DNA SEQUENCING

Total genomic DNA was extracted from approx-
imately 2 grams of leaf material of Hooglandia ig-
nambiensis McPherson & Lowry that was collected
in the field and preserved in a 2X CTAB salt-sat-
urated solution (Rogstad, 1992). Extractions were
performed using the modified CTAB method
Doyle and Doyle (1987) and were further purified
in cesium chloride/ethidium bromide gradients via
ultracentrifugation. The herbarium voucher for the

extracted DNA is P. P. Lowry II. G. McPherson, T.

Le Borgne & R. Pouytiela 5767 (MO), the type of

H. ignambiensis from New Caledonia.

The rbcL gene was amplified in one fragment us-
1994) and re-
verse primer 1460R (С. Zurawski, unpublished).

ing forward primer 71 (Wolf et al.,

The resulting product was sequenced using the
above primers as well as primers 427F, 997F,
515R, and 1081R (Goffinet et al., 1998). The PCR
reaction conditions used to amplify rbcL were 97?C
(4 min.); then 39 cycles of 94°C (30 sec.), 53°C (1
min.), 68°C (2 min.); followed by 72°C (7 min.). The
trnL-F region amplified with the forward primer C
and reverse primer F of Taberlet et al. (1991) and

was sequenced using their forward primers С & К
and reverse primers D € F. The PCR reaction con-
ditions used to amplify E were 97°C (4 min.):
then 39 cycles of 94°C (30 sec.). 48°C
72°C (1.5 min.): followed by 72°C (7 min.). All
ite PCR products were purified using the
Qiaquick РСК purific ation kit (Qiagen, Valencia,
USA.) P

cence-labeled according to the manufacturer's pro-

California, products меге fluores-

tocol using “Big-Dye” (Applied Biosystems) cycle
sequencing and were sequenced on an ABI version
377 automated sequencer.

The resulting sequences were proofed and edit-
ed, and double б ен pane were assembled
using Seqman 4.0 (DNAStar). Preliminary align-
ments were construc E using ClustalX (Thompson

=

et al., 1997) and then adjusted manually i
MacClade 4.05 (Maddison & Maddison, 2002). In-
sertions and deletions (indels) shared by two or
more taxa and greater than one bp in length were
coded and added to the data sets as additional bi-
nary characters. All sequences generated in this
study were deposited in GenBank and have acces-
sion numbers AY549639 (trnL, n, intron),
AY549040 (-F spacer), and AY549641 (rbcL).

PHYLOGENETIC ANALYSIS

Global rbcL analyses

To determine the phylogenetic position of Hoog-
landia among the angiosperms, its rbcL sequence
data were aligned to the 500-taxon rbcL data set of
Chase et al. (1993) (downloaded from Ken Rice's
Treezilla web site, http://www.cis.upenn.edu/~krice/
treezilla/) and analyzed using maximum parsimony
(MP) analysis. Because of the large size of the ma-
1428 шашы),

501 taxa, the Parsimony

—

trix
Ratchet (Nixon, 1999) was implemented in PAUP*
version 4.0b10 (Swofford, 2002) ad the setup
and batch files generated in PAUPRat (Sikes &
Lewis, 2001). Fifteen ratchet runs of 200 iterations
each were conducted, 15% of the characters
perturbed per iteration and equal starting weights.

with

The number of perturbed characters was chosen af-
ter running preliminary Ratchet searches with dif-
ferent numbers of perturbed characters (Sikes &
Lewis, 2001). All of the shortest, unperturbed trees
from each iteration were brought into PAUP using
the GET TREES FROM FILE option and filtered
to keep only those of shortest length, which were
then used to generate a consensus tree. To obtain
an estimate of support for individual branches,
1000 bootstrap (BS) replicates were run [with TBR
branch swapping, MULTREES option off, COL-
LAPSE option on, STEEPEST DESCENT option

268

Annals of the
Missouri Botanical Garden

< 79

Cephalotus drupacea - Cephalotaceae

Platytheca verticillata - Elaeocarpaceae

Bauera rubioides

Hooglandia ignamb

Eucryphia lucida

To remainder
of Angiosperms

76

Figure 1.

rbcL data set (sensu Chase et al.,

pee Oxalis dillenii - Oxalidaceae
— Averrhoa carambola - Oxalidaceae

A Amin of the 5096 ines consensus tree produced by 1000 resampling replicates of the 501-taxon
93). Significant bootstrap percentage values are shown above the branches. The
003).

shaded box estic members of C unoniaceae. Other family assignments are indicated (sensu APG, 2

off, and gaps treated as missing data]. Simulation
studies by DeBry and Olmstead (2000) indicated
that BS analyses using TBR branch swapping with
the MULTREES option set to off produce values
"essentially identical” to those in which the MUL-
TREES option is on while requiring less time to

run.

Focused rbcL and trnL-F analyses

After the approximate position of Hooglandia
was determined to lie among Oxalidales, rbcL and
trnL-F data were aligned to the data sets of Brad-
ford and Barnes (2001), which these authors had
used to evaluate relationships among the genera of
Cunoniaceae and which included several genera
from other families in Oxalidales as outgroups. We
used their data sets A (rbcL), B (trnL-F), and €
(rbcL and trnL-F), downloaded from TreeBASE (©
1994—2003, www.treebase.org), for the MP analy-
ses. For the rbcL and combined analyses, charac-
ters were unweighted and unordered, and 1000
heuristic search replicates were performed in
PAUP* version 4.0b10 [same options as before but
with the default setting of MULTREES option on].
Strength of support for individual branches was
again assessed using 1000 bootstrap replications
(Felsenstein, 1985). Because of time and computer
memory constraints, the nl data set was ana-
lyzed using the Parsimony Ratchet, which was im-
plemented as described above for the analysis of
the 501-taxon rbcL data set. To determine if the
rbcL and trnL-F data sets were combinable, Shi-
modaira-Hasegawa tests (Goldman et al., 2000;
Doust & Drinnan, 2004) were implemented in
PAUP*, with RELL optimization and 1000 repli-

cates.

-

RESULTS

GLOBAL rbcL ANALYSIS

Alignment of the 501-taxon data set, that is, the
sequences for 500 taxa used by Chase et al. (1993)
plus the sequence data from Hooglandia, resulted
in a data set with a total length of 1428 base po-
sitions; 798 characters were parsimony informative.
The Parsimony Ratchet resulted in 60 unique,
shortest length trees of 16,650 steps each (Consis-
tency Index (CI) excluding uninformative charac-
ters = 0.1017; Retention Index = 0.6390).
The strict consensus tree produced by the Parsi-
mony Ratchet places Hooglandia among a group of
genera belonging to Oxalidales. Figure 1 shows the
Oxalidales clade that resulted from MP analysis of
the 501-taxon rbcL data set. Hooglandia is strongly
supported (BS = 98%) as part of a clade containing
three sampled members of Cunoniaceae.
provides the authorities for the taxa in Figure 1.

=
=

FOCUSED rbcL AND trnL-F ANALYSES

rbcL analysis

The aligned rbcL data set, representing 38 taxa,
contained sequences with a total length of 1477 bp.
Maximum parsimony analysis resulted in three
trees. of steps (СІ excluding uninformative
characters = 0.5222; RI = 0.6774); 121 characters
were parsimony informative. The topology of the
strict consensus tree (not shown) was congruent
with the rbcL tree found by Bradford and Barnes
(2001) using their data set A (see their fig. 1), dif-
fering in the inclusion of Hooglandia. This newly
described genus (see McPherson & Lowry, 2004

Volume 91, Number 2
2004

Sweeney et 269

al.
Hooglandia DNA Analysis

Table 1.
and focused rbcL and trnL-F phylogenetic analyses.

Authorities for taxa used in the global rbcL

Outgroup taxa
Aristotelia en
Averrhoa carambol
Brunellia ln oet C uatrec.
Brunellia oliverii
Cephalotus dru arua Siebold & Zucc.
Cephalotus follicularis Labill.
Crinodendron ny Molina
Elaeocarpus reticulat tus Ridl.

Britton

Oxalis dillenii Jacq.
Platytheca verticillata Baill.
Ingroup taxa (Cunoniaceae sensu Bradford & Barnes.
2001)

Ackama paniculosa Beuzev. & С. T. White
Acrophyllum australe (A. Cunn.) Hooglan d

Acsmithia elliptica (Vieill. ex Pamp.) ит
Anodopetalum ко (Hook.) Hook.
Bauera rubioides Andrew

Caldeluvia panic 55 D ‘Don

Callicoma serratifolia Andi

Guillaumin

I
gn. ۰ Gris)
h

Schltr.

is
—
~
=
`~
—
—
=
— 2
I
— ^
E:
wn
—
ч
—
=
P
>
M
—
~
e
—
=
pz
=

1
-seudoweinmannia in oum (F. Muell.) Engl.
P glabra Se а

Spiraeopsis calehi a Miq.

5 ura ieanthe тит samoense A. Gray

Weinmannia bangit Rusby

Weinmannia ME arlensis E ex Ser.
Weinmannia raiateer

W.
Vesselowska rubifolia (Е Muell.) 2-5

was placed їп а subbasal clade of Cunoniaceae with
strong support (BS = 100%).

trnL-F analysis

The total length of the aligned sequences in the
data set was 1282 ;
ing time, Cunoniaceae taxa included in the trnL-F
data set of Bradford and Barnes (2001) (data set B)

but absent from their rbcL data set were excluded.

=

trnL-F Го decrease comput-

resulting in a reduced sample of 36 taxa. The ex-
cluded taxa were all from well-supported genera
that had multiple representatives in the original
data set. Alignment of the trnL-F sequences re-
quired 95 indels, of which only 27 were parsimony
informative and greater than 2 bp in length. The
27 parsimony-informative indels were coded as bi-
nary characters and appended to the end of the

molecular data set. Hooglandia did not have either
the “Big” or “Small” deletions as identified by
Bradford and Barnes (2001) for trn L-F.
Ratchet resulted in 2996 shortest-length
The bootstrap consensus tree (not shown) re-

The Parsi-
mony
trees.
sulting from the analysis of the trnL-F data was
visually congruent with the consensus tree resulting
from the analysis of data set B in Bradford and
Barnes (see their fig. 2, 2001), differing notably by
the exclusion of certain taxa (as mentioned above)
and the inclusion of Hooglandia, which was again
placed within a subbasal clade of Cunoniaceae (BS

100%).
Combined rbcL + trnL-F analysis
Shimodaira-Hasegawa (SH) tests (Goldman et al..

2000) were employed to determine if significant dif-
ferences existed in the topologies produced by the

rbcL and trnl-F data sets (e.g.. Doust & Drinnan.
2004). To test for effects of differing topologies

within a data set, trees from an unconstrained anal-
ysis were compared to trees constrained by either
of the topologies derived from the other data set
and the combined data set. Specifically. the topol-
ogy produced by an unconstrained analysis of the
rbel, partition was compared against the 70% boot-
strap consensus trees produced by MP analysis of
the trn L-F data set and by analysis of the combined
гет
was performed on an unconstrained trnL-F topology

data set. The reciprocal comparison
tested against the 70% bootstrap consensus trees
produced by MP analysis of the rbcL data set and
by analysis of the combined rbcL/rnL-F data set.
In all such tests no significant differences were
found (P > 0.05), indicating that there is no con-
flict between the phylogenetic signal derived from
each data set. The SH tests thus indicated that the
data sets could be combined for further analysis.
The length of the sequences in the combined
rbcL/trnL-F. data set was 2695 bp. Maximum par-
simony analysis resulted in 15 trees of 770 steps:
222 characters were parsimony informative (CI ex-
0.6009: RI
0.7014). One of the shortest-length trees is shown

cluding uninformative characters —

in Figure 2, with branch lengths indicated. Figure
3 shows the topology of the 5096 strict consensus
of the bootstrap analysis as legend). The strongly
supported branches (BS > 70%) are the same as
those produced by jack of data set C of Brad-
ford and Barnes (see their fig. 3, 2001). Again.
Hooglandia was placed in a subbasal clade of Cu-
100%).
| provides the authorities for the taxa in Figures 2

and 3.

noniaceae with strong support (BS = Table

270 Annals of the
Missouri Botanical Garden

17__ Caldcluvia paniculata

s ee ra
Eucryphia coi

la

4
7 EM
15 11 Geissois b
13 Ó. Pseudowein
23 Gillbeea ac
9
10
20
17
34 Hooglandia і
27 42 2 Acsmithia elliptica
ES Spiraeanthemum
35 + Brunellia colombiana - Brunelliaceae
16 | ut Brunellia oliverii - Brunelliaceae
m Cephalotus follicularis - Cephalotaceae
44 — Crinodendron patagua - Elaeocarpaceae
Elaeocarpus reticulatus - Elaeocarpaceae

Aristotelia chilensis - Elaeocarpaceae

re 2. One of 15 minimum- че trees of 770 steps produced by maximum parsimony analysis of the combined
AE data set. Branch lengths are shown above the branches. The shaded box surrounds members of Cunoniaceae,
as circumscribed by Bradford and Bones (2001). Other family assignments are indicated (sensu APG, 2003).

Volume 91, Number 2
2004

Sweeney et al.
Hooglandia DNA Analysis

Ackama paniculosa
Spiraeopsis celebica —

95
Caldcluvia paniculata |

pues Acrophyllum australe i

Eat Eucryphia cordifolia

ps Callicoma serra
Ll :

Codia discolor

66 Cunonia atrorubens :

Weinmannia

uon еш

Weinmannia raic

uonopoq 519

Weinmannia Бапай —

Vesselowskya rubiſolia

100

Pullea glabra
Geissois benthamii

Pseudoweinmannia la

un
N

Gillbeea adenopetala
Anodopetalum bigle ndulc
Platylophus trifoliatus

Ceratopetalum gum |
Bauera rubioides
Davidsonia pruriens

әрел=у [eseg

Hooglandia ignan
== Acsmithia le

р Spiraeanthemum ва

Brunellia colombiana - Brunelliaceae

Brunellia oliverii - Brunelliaceae

Cephalotus follicularis - Cephalotaceae

Aristotelia chilensis - Elaeocarpaceae

Figure 3.

. Numbers above branch

F) and e Basal
APG, 2003).

While Hooglandia is clearly a member of Cu-
noniaceae, its exact position within the family is,
however, equivocal. In both the MP and 50% boot-
strap consensus (Figs. 2, 3) trees for the combined

Crinodendron patagua - Elaeocarpaceae

———
—
ses

Elaeocarpus reticulatus - Elaeocarpaceae

The 50% bootstrap consensus tree produced by 1000 resampling replicates of the combined rbcL/trnL-
ue e sh

aded box surrounds members of
xa possessing the “Small” and “Big” deletions (trnL-

Grade of Bradford and Barnes (2001) are ant Other family assignments are indicated (sensu

data, Hooglandia is placed in a large clade that is
sister to the basal-most clade (comprised of Acsmi-
thia and Spiraeanthemum) in the family. Hooglan-
dia is then sister to the remaining members of the

272

Annals of the
Missouri Botanical Garden

family, although this relationship is weakly sup-
ported (Fig. 3, BS = 56%). If this branch is col-
lapsed, the position of Hooglandia is unresolved
within the Basal Grade sensu Bradford and Barnes
(see their fig. 2, 2001: 361, and Fig. 3 herein).

DISCUSSION

PHYLOGENETIC POSITION OF HOOGLANDIA

>
—
2

he primary goal of the molecular phylogenetic
analyses presented in this paper is to establish the
placement of a newly discovered plant from New
Caledonia, described by McPherson and Lowry
(2004) as Hooglandia ignambiensis. The results ob-
tained from the analysis of rbcL and trnL-F se-
quence data strongly support the inclusion of Hoog-
landia within Cunoniaceae. Hooglandia falls above
the first-branching clade within the family, com-
prised of Acsmithia Hoogland and Spiraeanthemum
. Gray, well within the bounds of the family as
circumscribed by Bradford and Barnes (2001).
Hooglandia possesses interpetiolar stipules,
which may represent the only clear synapomorphy
370)
described most basal Cunoniaceae as having bra-

for Cunoniaceae. Bradford and Barnes (2001:

chyparacytic subsidiary cells in the leaf epidermis
and suggest that this condition may also be a syn-
apomorphy for the family. Unlike other basal Cu-
noniaceae, Hooglandia has what are best described
as anomocytic subsidiary cells, although they do
not fit neatly into any described stomatal type (sen-
su Metcalf & Chalk, 1974). Epidermal peels from
the abaxial surface of the middle of two leaflets of
the type specimen of H. ignambiensis were exam-
ined during the course of this investigation. The
guard cells (average length of 12.2 jum, m number
or N — 20, standard deviation or s.d.
slightly everted and partly overlie the soning
4 to 7 (N =

lygonal subsidiary cells, which are similar in de

are

20, average = 5.25, s« po-
to the surrounding epidermal cells, differing only
in their smaller size (average length of 8.65 jum (М
= 20, s.d. = 1.93) vs. 12.73 jum (N = 20, s.d. =
3.1) and average width of 6.65 jum (N — 20, s.d.
= 1.87) vs. 9.58 uum (N = 20, s.d. = 2.29)). There

seems to be some discrepancy in the scoring of

1 Cunoniaceae, as

subsidiary cell arrangement i
Dickinson (1975) classified the stomatal type for
many genera differently than Bradford and Barnes
(2001). This disagreement suggests that there may
be variation in stomatal types within species and
genera of Cunoniaceae and that caution should be
exercised when using stomatal type as a systematic
character within the family.

Another feature supporting the

placement of

Hooglandia in Cunoniaceae is its possession of
starchy endosperm, a feature shared among all
members of the family but absent in the mature
ovules of most other members of Oxalidales (except
Oxalidaceae and Brunellia Ruiz & Pav.) and un-
usual within Rosids (sensu APG, 2003). Starchy
endosperm is not present in Sapindales, one of the
groups to which it was initially thought that Hoog-
landia might belong.

Other characters that. support the inclusion of
Hooglandia in Cunoniaceae (but do not necessarily
represent. synapomorphies for the family) include
opposite imparipinnately compound leaves, panic-
ulate inflorescences, tetramerous flowers, a diplos-
temonous androecium, an intrastaminal disk, and a
superior bi-ovulate ovary.

EVOLUTIONARY IMPLICATIONS

Because the sister relationship of Hooglandia to
the remainder of the genera within Cunoniaceae
(except for the basally branching clade comprising
Acsmithia + Spiraeanthemum) is only weakly sup-
ported, it would be premature to base any interpre-
tations of character evolution on the topology re-

vealed by the present analyses (Figs. 2, 3).
Nevertheless, the position of Hooglandia among
basal Cunoniaceae is supported by its possessing
tricolporate pollen, secondary veins terminating
teeth on the leaflets, and the presence of anthers
with a thecal connective protuberance (see fig. 5 in
Bradford & Barnes, 2001).

Specialists working on Cunoniaceae agree that
Hooglandia resembles Aistopetalum and that it
might therefore be closely related to it (Barnes &
Hopkins, pers. comm.). A sister relationship be-
tween Hooglandia and Aistopetalum is also weakly
supported by cladistic analysis of morphological
data (Bradford & Sweeney, unpublished data). |
these morphological analyses, Hooglandia and his
topetalum are sister to Davidsonia F. Muell., and
these three taxa form a clade occupying a subbasal
position between a clade containing Acsmithia and
Spiraeanthemum and its sister clade comprising the
rest of the family. Characters supporting a close
relationship between Aistopetalum, Hooglandia,
and Davidsonia include imparipinnate leaves, pa-
niculate inflorescences, and indehiscent drupa-
ceous fruits. Unfortunately, extraction of DNA from
herbarium specimens of Aistopetalum has so far
failed. Relationships among the Basal Grade of Cu-
noniaceae (see fig. 2 in Bradford & Barnes, 2001;
Fig. 3 herein) are poorly understood, and this sit-
uation draws attention to Aistopetalum as a priority

Volume 91, Number 2
2004

Sweeney et al. 273

Hooglandia DNA Analysis

genus for further molecular systematic investiga-
tion.

dioecious, as
& Gris,
and Weinmannia L.,

Hooglandia 15

Pancheria Brongn. Vesselowskya Pamp.,
which belong to a derived
clade within Cunoniaceae (Figs. 2, 3). The position
of Hooglandia relative to the clade containing
Pancheria, Vesselowskya, and Weinmannia would
suggest that dioecy arose in parallel in these two
clades.

Hooglandia is unique within Cunoniaceae and
Oxalidales in its possessing a unicarpellate (or per-

—

haps pseudomonomerous) ovary versus 2(3-14)-
carpellate ovaries in the rest of the family and order
(McPherson & Lowry, 2004). It is also unique with-
in the family in its possessing bilaterally symmet-
rical, drupaceous fruits.
THE ROLE OF MOLECULAR DATA IN DESCRIPTIVE
SYSTEMATICS

Several recent advances have had tremendous
impact on the field of plant systematics, including
the increased ease of obtaining DNA sequence
data, improvements in computer technology, and
the development of more powerful phylogenetic
2000; Crawford, 2000: Ste-
vens, 2000). While these changes have provided

software (Chase et al.,

important new insights into the evolutionary rela-
tionships among organisms and have prompted sig-
nificant modifications to modern classification sys-
tems of flowering plants, molecular techniques have
been used only sparingly by plant systematists
when describing new taxa. This is not surprising,
as the taxonomic group to which most newly dis-
covered plants belong is often readily and accu-
rately inferred from its phenotype. However, some
authors have raised the point that taxonomic ex-
pertise is unfortunately vanishing and that molec-
ular data may have to play a more substantial role
2002: Hebert

Molecular. data

—

in descriptive systematics (Godfray.
2003; Tautz et al., 2003).

have already been used to identify and describe

et al.,

entities in groups that present a limited number of
phenotypic characters or in which features are am-
biguous or hard to interpret, such as nematodes
(Floyd et al., 2002). bacteria (Jonasson et al.,
2002), and fungi (Redecker et al., 1997). In what
was touted as one of the first examples of such an
application of molecular data in flowering plants,
Garnock-Jones et al. (1996) assessed the family-
level placement of an unknown sterile plant col-
lected in New Zealand, concluding that it could be
an unnamed new genus of Cunoniaceae or a dwarf
mutant of Weinmannia racemosa L. f. Subsequently,

species of

Bradford and Barnes's (2001) phylogenetic analyses
suggested that the particular accession. examined
by Garnock-Jones et al. (1996) may indeed belong
to H. racemosa. Although it is uncommon among
flowering plants to encounter cases where the re-
lationships of an organism are uncertain, when they
do arise, molecular techniques offer an ideal way
to evaluate relationships quickly and efficiently. In
the case of Hooglandia, it took some 12-15 hours
to extract, amplify, sequence, and analyze the rbcL
and trnL-F data sets. By contrast, it was not pos-
sible using morphology to place ч with
confidence even at the ordinal level. In this case,
molecular data proved to be indispensable for rec-
ognizing that Hooglandia is a member of Cunoni-

aceae.
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APG ү pe чө Phylogeny Group).
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rbcL sequences. Molec. Phylogenet. Evol. 3: 383—392.

EVOLUTION OF

VERONICEAE: A
PHYLOGENETIC
PERSPECTIVE!

Dirk C. Albach,?? Ma. Montserrat
Martínez-Ortega,* Manfred A. Fischer,?
and Mark W. Chase?

ABSTRACT

enus Veronica (Plantaginaceae, formerly Se а eae) is well known for its pede ed corolla tube in an

le g
otherwise long- tubed family. Similar character reversals

trnL-F s

We here use Veronica in a wide sense including the Hebe е x, Syn
on comparison with results from the molec ular analyses, we in
. The terminal ida. тсе was probably lac king i in the ancestor of Vorons ‘eae

with two losses and at least two re gain

by earlier authors match

of Veroniceae with other base numbers e

states thought to be „в
are found in inflorescence morphology, embryology, and diete idi We have used 1
eee e data in separate and combined data sets to explore character еа in Veronica and related genera.

with little conflict results from the molecular analyses
as tne an of micropylar endosperm haustoria. Finally, chromosome hE
volving several times in par

utside Veronica
thyris, Besseya, and Pseudolysimachion. Based
er the rosette habit to be ancestral in the tribe Veroniceae

wers evolved in pi

do embry ologic: al 7 a ‘ters such
s likely to be е X =
alle 1. Similarities of the inferred anc r character

the ancestor

states with those from the outgroups Plantago and Digitalis are discus

Key words:

ed.
character evolution, ITS, molecular systematics, trn L- F, " Veronic a, Veroniceae.

The genus Veronica L. (Plantaginaceae sensu

APG,

terized by its more or less short-tubed to subrotate

2003; formerly Scrophulariaceae) is charac-

and subactinomorphic flower, whereas most of its
relatives in Lamiales (sensu APG, 2003) have long-
tubed zygomorphic flowers. Veronica is an example
of a taxon with generally derived characters in
which many species developed character states oth-
erwise considered plesiomorphic. These character
reversals are not only found in the flower but also
in inflorescence morphology, embryology, and kar-
vology. The following reversals occur in at least
some species: the corolla tube becomes reduced to
an almost choripetalous state; a zygomorphic flower
becomes almost actinomorphic; the thyrse becomes
reduced to a raceme; corolla lobes become reduced
from five to four by fusion of the adaxial lobes. The
same can happen in the calyx. Stamen number be-
comes reduced from four to two. Endosperm haus-
toria become reduced from four uninucleate cells
to one bi- or uninucleate cell. Such character tran-
sitions have drawn the interest of scientists for de-

cades (e.g., Lehmann, 1918; Hamann, 1960:
Kampny & Dengler, 1997). The differentiation be-
tween terminal and strictly lateral inflorescences
and between annual and perennial life histories, for
example, has been considered a major division in
1977). Mo-

lecular data now give the opportunity to evaluate

the genus (Rómpp, 1928; Elenevskij,

previous hypotheses of character evolution in the
tribe Veroniceae. We have already discussed some
of these characters in previous publications (Al-
bach & Chase, 2001; Albach et al.,
also Martínez-Ortega & Rico, 2001) and shown the
non-informativeness of the inflorescence and Ше

in press a; see

history characters toward a taxonomic revision of
the genus. We have therefore proposed a revised
classification for Veronica (Albach et al., in press

b) that includes the Hebe complex, Synthyris, Bes-

seya, and Pseudolysimachion. In this circumscrip-

The Hebe

complex is divided into two subgenera, the Austra-

tion, Veronica includes 13 subgenera.

lian species of Veronica and Derwentia, and the

New Zealand core-Hebe group. Synthyris and Bes-

! We thank the Studienstiftung des deutschen Volkes for a doctoral scholarship to DCA and the Spanish Ministerio

de Cien

Junta de Castilla a y León and the European Union (FSE) t

ncia y Tecnología for a postdoctoral pt (programa FPI) to MMO. This
thro

work was partially supported by the
ugh the research project SA117/01

Department of Higher Plant Sy stematics, Minus of Botany, University of Vienna, Rennweg 14, 1030 Wien, Austria.

albach@gmx.net; m.a.fisc ош ас
3 Jodrell Laboratory, Royal Botanic саш

Richmond, Surrey, TW9 3DS, United Kingdom

.m. AN org.uk.
l.e

Departamento de Botánica, 1 niversidad de Salamanca, E-37007 Salamanca, Spain. mmo@usa

ANN.

MissouRi Bor. GARD. 91: 275-302. 2004.

276

Annals of the
Missouri Botanical Garden

seya are combined in subgenus Synthyris, while
Pseudolysimachion is reduced to subgeneric rank.
Subgenus Veronica includes many Eurasian and Af-
rican montane to alpine species with a base chro-
mosome number of x = 9, whereas those with x =
8 are found in subgenus Stenocarpon. Subgenus
Pentasepalae includes most southwest Asian spe-
cies along with European species from dry mead-
ows. Subgenus Beccabunga includes the relatives
of V. beccabunga, V. serpyllifolia, and the annual
relatives of V. acinifolia. Subgenus Chamaedrys in-
cludes V. chamaedrys and relatives along with the
annual V. arvensis and V. verna. Purely annual sub-
genera are subgenus Cochlidiosperma (V. hederifol-
subgenus Pelli-

~

ia, V. cymbalaria, and relatives),
dosperma (V. triphyllos and relatives), subgenus
Triangulicapsula (V. grisebachii), and subgenus Po-
cilla (V. agrestis and V. biloba with relatives). We
will use Veronica in this wide sense in the follow-
ing, although sometimes terming it Veronica s.l. for
special emphasis of this wider circumscription.
New molecular data for the nuclear ribosomal ITS
and the plastid trnL-F regions for more taxa than
in previous analyses (Albach & Chase, 2001;

bach et al.,
diversity in the genus and related genera in Veron-

in press a), representing most of ii

iceae, give here the opportunity to analyze char-
acter evolution in Veronica more thoroughly.

MATERIALS AND METHODS

We have sampled 71 taxa of the Veroniceae rep-
resenting most of the diversity in the tribe with the
exception of species from the Southern Hemisphere
(the Hebe complex), which represents a radiation
of its own (species including authorities are listed
in Table 1). Taxon sampling among subgenera is
unequal, with taxon density ranging from 10 to 60%
of the species to reflect infrasubgeneric diversity.
An additional 11 taxa were included to represent
taxa related to Veroniceae following results from
previous analyses (Albach & Chase, 2001; Olm-
stead et al., 2001). Oreosolen, Lafuentea, and Sib-
thorpia have been used as outgroups. The analysis
extends the sampling of the previous analysis of ITS
(Albach & Chase, 2001) and trnL-F (Albach et al.,
in press a) with 43 new IT'S sequences and 32 new
trnL-F sequences. We present matching data sets
with DNA from the same specimen for both regions
with the exception of Veronica glauca, V. abyssinica,
Parahebe vanderwateri, Plantago lanceolata, and P.
major (vouchers listed in Table 1). Taxon sampling
in the Hebe complex has been restricted because
an evaluation of these species is presented else-

where (e.g., Wagstaff et al., 2002). We have used

the classification of Albach et al. (in press b) of
Veronica including Synthyris, Besseya (both consid-
ered together as Veronica subg. Synthyris), and the
Hebe complex (subgenera Derwentia and Hebe), al-
though for species in the Hebe complex we retained
their combination under their other genus name be-
cause new combinations have not been made for all
made for all

species. Voucher

specimens were
plants used in this study (Table
DNA EXTRACTION, AMPLIFICATION, AND
SEQUENCING

The protocol followed previous studies (Albach
& Chase, 2001; Albach et al., a). Total
genomic DNA was extracted from herbarium ma-
terial and silica-gel-dried leaf samples according to
the 2x CTAB procedure of Doyle and Doyle (1987)
and then washed twice with 70% ethanol. DNA pel-

in press

lets were dried and resuspended in TE-buffer.
The trnL intron, 3'exon, and trnL-F spacer (here-
after trnL-F) were amplified with. primers c and f
of Taberlet et al. (1991). ITS
plified and sequenced using the primers 17SE (Sun
. 1994) and ITS4 (White et al., 1991). In con-
trast to previous amplifications, we did not add
DMSO, which facilitates amplification when there
are problems with secondary structure, because we
found it inhibits PCR when DNA quality was low.
PCR products were run on a 1.0% TBE-agarose
gel, cut out of the gel, and cleaned using QIA-
quick™ PCR purification and gel extraction kit
(Qiagen GmbH, Hilden, Germany) following the
manufacturer's protocols. Sequencing reactions (10
the Taq Dye-

sequences were am-

pl) were carried out using ] p
Deoxy Terminator Cycle Sequencing mix (Applied
Biosystems Inc.). Reactions were run out on a
Prism 377 automated sequencer (Applied Biosys-
tems Inc.), and both strands were sequenced. Se-
quences were assembled and edited using Se-
quence Navigator™ (Applied Biosystems Inc.).
Assembled sequences were manually aligned prior
to analysis. All sequences have been deposited in
GenBank (accession numbers listed in Table 1).
Aligned sequence matrices are available from DCA
and MWC by request.

SEQUENCE ANALYSIS

Insertions and deletions are frequent in both
DNA regions (ITS and trnL-F). In a conservative
approach we scored gaps as mcis н thus re-
moving them from the analysis.
analyzed with PAUP* 4.0b7-10 үче 1998)
using heuristic parsimony search methods. Both
simple and random (with 10 replicates) taxon ad-

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Evolution of Veron

Albach et al.

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‘penunuor) т әре,

281

Albach et al.

Volume 91, Number 2

2004

Evolution of Veroniceae

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“panuquo”) `1 әү],

282

Annals of the
Missouri Botanical Garden

dition with tree bisection reconnection were con-
ducted multiple times (usually 3 times) with
MulTrees (keeping multiple shortest trees) in effect
with no tree limit. Bootstrap percentages were es-
timated using 500 replicates and SPR-branch
swapping with a maximum of 20 trees per replicate
to assess support for relationships. Branch support

was also estimated with a decay (Bremer support)
analysis using Autol
1998) with simple taxon addition and TBR branch

ecay vers. 4. ;riksson,
swapping, saving all most parsimonious trees. A
third method to estimate confidence in the tree is
based on Bayesian statistics as implemented in the
computer program MrBayes 2.01 (Huelsenbeck &
Ronquist, 2001). We used default settings with a
GTR «T likelihood model and started the analysis
from a random tree. Four Markov chains, three
heated and one cold chain, were run simultaneous-
ly for 200,000 generations each and the current
tree saved every 10 generations. To check that sta-
tionarity had been reached we plotted the likeli-
hood values per generation and repeated the sim-
The first 3000 generations were
A majority-rule consensus

ulation twice.
discarded (burn-in).
showing all compatible groupings of the resulting
19,700 trees was then used to show approximate

ps

posterior probabilities that the clade exists. Fo
character analysis, we have used MacClade 3.06
(Maddison & Maddison, 1992).

Incongruence between nuclear and plastid DNA
sequences is a widespread phenomenon and may
have various causes (Wendel & Doyle, 1998), for
example, hybridization and introgression (Soltis et
al., 1996). The data sets were therefore analyzed
both separately and in combination to test for con-
gruence. Bootstrap support was estimated for sep-
arate and combined data sets. We here do not dis-
cuss results of soft incongruence (sensu Seelanan
et al., 1997) in which the two data sets show dif-
ferent relationships but only one gives more than
50 BP (bootstrap percentage) for this relationship.
Those cases herein in which the individual analy-
ses support different results, however, indicate
sources of true incongruence and will be discussed
in more detail.

One reason for incongruence may be homoplasy
in at least one data set. CT transitions are the most
common nucleotide change in ribosomal DNA due
to the spontaneous deamination of C to U occurring
in nature, a mutation that in contrast to other mu-
tations maintains RNA base pairing (Vawter &
Brown, 1993; Hershkovitz et al., 1999) and
therefore, more likely to be retained. Soltis and Sol-
tis (1998) investigated the effect of down-weighting
transversions in the analysis of 18S rDNA. They

found, however, only a decrease in the resolution
of the strict consensus trees and concluded that a
down-weighting of transversions is probably not
worth the effort of extra computer time required to
conduct some of the analyses (Soltis & Soltis, 1998:
205). We have analyzed our ITS data set separately
and combined with the trnL-F data set parallel to
the unweighted analysis with CT transitions re-
moved from the data set using a step matrix to test
the effect of CT transitions in ITS on the results.

RESULTS

The analysis of the nrITS-region included 915
characters, 335 of them potentially parsimony in-
formative, and resulted in 864 most parsimonious
trees of 2199 steps with a consistency index (CI)
of 0.37 and a retention index (RI) of 0.66 (Fig. 1).
The results of the analysis of ITS are very similar
to those by Albach and Chase (2001). However,
resolution of the major subclades of Veronica is low-
er. Paederota, Synthyris, and the Hebe complex are
nested within Veronica. Veronica subg. Beccabunga
is the first branching subclade in Veronica. The po-
sition of subgenus Cochlidiosperma differs between
NA regions. It is sister to
subgenera Pentasepalae, Pocilla, and Chamaedrys

the analyses of the two
in Albach and Chase (2001), whereas it is sister to
the subgenus Pseudolysimachium here (Fig. 1).
The analysis of the trnL-F including 1336 char-
acters, 333 of them potentially parsimony infor-
mative, was run several times with a tree limit of
1000 trees. Trees from one replicate were saved.
They 1 wow steps with CI — 0.66 and RI
— 0.81 (Fig. 2). The results of the analysis of the
trnL-F region are very similar to those of Albach
et al. (in press a). Resolution of the major subclades
in Veronica increased, in contrast to results from
ITS. Paederota and Picrorhiza are sister to Veronica
in both analyses, whereas Synthyris and the Hebe
complex are again nested within Veronica. Subge-
nus Veronica is the first branching subclade in Ve-
ronica (Fig. 2), whereas it was in a basal polytomy
in Albach et al. (in press a). The Hebe complex is
again sister to subgenera Pentasepalae and Pocilla.
The favored method of examining incongruence
among two or more data sets is comparison of sep-
arate and combined results on a node-by-node ba-
sis, specifically bootstrap support and resolution.
Taxa of Veronica that appear in different positions
in the two separate analyses are not well supported
in both analyses and are therefore not considered
true incongruences but most likely due to sampling
error (Reeves et al., 2001). This was also confirmed
by incongruence tests performed by Albach and

Volume 91, Number 2

Albach et al.
Evolution of Veroniceae

283

(sherpa ga
Busia: ea . 2 ola
lobul

OO
Qo

Sa

OO
-

on
5 а chamaed С
угол M as ашы Сосһ
|

eronica
Veronica coo
e

li
eronica o m
Veronica Са Deuces

Ф

Vero 8 a на

Veroniceae
x

*

Veronica ا‎

Veronica B
рава Чо Obata

Veron а (лор
ronica eccabunga
eronica heureka
51 |

castrum li
99

ai fa ts. angusti racteata
gots stólonife

Subgenus
Pentasepalae

Subgenus
ocilla

| Subgen
Cham а
lidiosperma)
ubgenus
Pellidosperma

ubgenus
Stenocarpon

g
2 eee ee

ubgenus Synthyris

Subgenus
Veronica

Paederota

ubgenus
Pseudolysimachium

Subgenus
Cochlidiosperma

Subgenus
Beccabunga

| wulfenioid
grade

Figure l. Strict consensus tree of 864 most parsimonious trees of the analysis of the ITS data set. Numbers above
the branches indicate bootstrap percentages ie b. analysis of equally weighted characters. Numbers below the branches
of characters exclu qua CT transitions. Re lationships to the right of the
itionships found in ene 3 analyse t not found in any most parsimonious tree. C
0.37; RI = 0.66. Бя ‘bolkardaghensis” is an abbreviation for ranita bombycina subsp. bolkardaghensis.

284 Annals of the
Missouri Botanical Garden

Oreosolen wattii
Lafuentea rotundifolia

57 Plantago uniflora

lia
Kardaghensis Subgenus
огае Pentasepalae

V отса Dersic E Subgenus
eronica campylopo ;
ronica п serrata | Pocilla
Veronica amo па

Barahebe v rubritoli Hebe complex

b
eronca thess puer. Subgenus Triangulic.

үа arvensis Subgenus‏ جج
ни‏ |

S3
5
®

2

67 L— Veronica aie
64| 100 y veronica 1515 lobata
eronica 1 MM Subgenus Synthyri
09 OR ca ¡apra ion nga 59
l97 —

vero oniga сеи

ubgen
97 Veronica бе 1 1
99 деп ia ر‎ En
99 ve ee fo de
eronica ong it ia
100 E veronica
аа vero nica 0 10 5

99 j увора paupas ulasa
— Veronica Byssinica
Veronica serora

5

ica
Veronica Ja Jat JOrjensis
omen orrisonicola Sub
nica officinalis ubgenus
VA al hy Veronica

Veroniceae

100 p peo

E
i с,
— tet 100 а ofis ап ш wulfenioid
olis std onien А nicum grade
e.-- veronicastrum vi
100— Veronicastrum stemonostachys
— Veronicastrum liukiuense

Figure 2. Strict consensus tree of 1000 most p trees of the analysis of the trnL-F data set. Numbers
above the branches indicate bootstrap percentages for the analysis of equally we sighted characters. Re ‘lationships to the
right of the ie ies names show relationships found in the bootstrap analyses but not found in any most parsimonious

. CI = 0.66; КІ = 0.81. Veronica “bolkardaghensis” is an abbreviation for Veronica bombycina subsp. bolkardagh-
ensis.

Volume 91, Number 2
04

Albach et al. 285

Evolution of Veroniceae

Chase (in press). However, the relationships among
the members of the wulfenioid grade appear to be
cases of true incongruence, with results from ITS
and trnL-F differing strongly due to hybridization
(Albach & Chase, in press). Based on the lack of
true incongruence among members of Veronica, we
decided to combine the matrices and to discuss dif-
fering inferences based on the two different hy-
potheses, if appropriate.

The combined data matrix included 2251 char-
acters, 668 of them potentially parsimony infor-
mative. The analysis resulted in 112 most parsi-
monious trees of 3431 steps (CI = 0.47; RI = 0.70:

ig. 3). Tree scores estimated separately for the two
individual partitions differ considerably. ITS ac-
counts for 2219 to 2222 steps, whereas trnL-F ac-
counts for 1210 to 1213 steps of the total 3431
steps. The CI of the ITS partition was 0.37 and the
КІ = 0.65, whereas for the trnL-F partition СІ
0.64 and RI = 0.80.
those from separate analyses previously published
(Albach & Chase, 2001; Albach et al., in press a).

The combined analysis shows better resolution and

These values are similar to

higher bootstrap support than the analysis of the
two partitions alone. In some patterns it resembles
the results from the ITS analysis (e.g.. Hebe com-
plex sister to subg. Stenocarpon), whereas in others
it resembles the trnL-F analysis (e.g.. Paederota
sister to Veronica s.l.). The sister-group relationship
of subgenus Synth yris and subgenus Beccabunga is
not found in either strict consensus tree of the in-
dividual regions (Figs. 1, 2). Support for the mono-
phyly of subgenera Stenocarpon and Cochlidiosper-
ma is increased compared with analyses of separate
data sets. Generally, we can state that all strongly
supported clades of the combined analysis repre-
sent relationships supported consistently in all in-
dividual analyses.

CT transitions are by far the most common char-
acter change in the data set (815 steps compared
with 427 steps for AG transitions and 348 steps for
AC transversions) as reported for rDNA generally
(Vawter & Brown, 1993; Hershkovitz et al., 1999),
although they are not the most frequent nucleotides
(21.4% A, 28.6% C, 29.0% G, 21.1%

CT transitions are not only the most common char-

. However,

acter change, but also have the lowest consistency
index, although the effect is not large. The exclu-
sion of CT transitions from the data leads to a slight
increase of the Cl and RI (0.37 to 0.41 and 0.66
to 0.68, respectively). The exclusion of AG transi-
tions (CI = 0.33: RI = 0.63) and AC transversions
(Cl = 0.33: RI = 0.64) leads to a decrease in the
tree scores. Our investigation of the effects of re-
moving CT transitions corroborated the results of

Soltis and Soltis (1998) in 185 rDNA of mainly
decreased resolution. The analysis with this pruned
ITS data set had to be run with a tree limit of 5000
trees, which had 1267 steps with CI = 0.42 and
RI = 0.69 (Fig. 4). Branch support similarly de-
creases after removal of CT transitions, although a
few relationships find increased support (e.g.. sis-
ter-group relationship of V. donii and V. triphyllos,
from 74 BP to 97 BP). These relationships concern
especially species groups in which taxon sampling
is poor, such as Veronica subg. Beccabunga, thus
preventing the detection of homoplasy in the phy-
logenetic analysis. All supported clades of the ITS
analysis with a conflicting supported relationship in
the trnL-F analysis are not supported in the anal-
ysis of ITS with removed CT transitions, with the
exception of the Veronica + Paederota + Wulfenia
clade

Consequently, support for clades in the com-
bined analysis with CT transitions removed from
the ITS partition is higher for many clades than in
the equally weighted combined analysis because of
the greater weight of trnl-F characters. Those
clades with lower support represent mainly cases
in which ITS with removed CT transitions and tral-
F are not variable enough. An especially notewor-
thy relationship in this combined analysis with CT
transitions removed from the ITS partition is the
sister-group relationship of subgenus Veronica to
the rest of Veronica (no support in the combined
analysis, 64 BP in trnL-F, 87 BP in the combined
analysis with CT transitions removed from the ITS
partition).

Bootstrap analysis (Fig. 3) and Bayesian statis-
tics support mostly the same relationships (Fig. 5)
with posterior probabilities being higher than boot-
strap percentages in all cases in which bootstrap
percentages are below 95, as noted by Buckley et
al. (2002). However,

ences. Bayesian maximum likelihood does not sup-

there are some notable differ-

port the monophyly of the combined clade of sub-
genera Cochlidiosperma and Pellidosperma and
supports positions of subgenus Synthyris and Ve-
ronica scutellata as shown in the analysis with CT
transitions removed from the ITS partition (Fig. 4).
albeit with probabilities below 90%. Most interest-
ing are the inferred relationships in the wulfenioid
grade. Here (Fig. 5), Bayesian maximum likelihood
supports the position shown in the analysis of ITS
(Fig. 1) rather than the trnL-F (Fig. 2
bined analysis (Fig. 3). The analysis with CT tran-
sitions removed from the ITS partition (Fig. 4) was

and com-

—

largely unresolved in the wulfenioid grade. Never-
theless. we base our following discussion on the

simple combined analysis (Fig. 3) but discuss in-

286

Annals of

the

Missouri Botanical Garden

Veronica
76
Pal

not present in
strict consensus tree

Strict consensus tree of 112 most p

t
isi IS and vim -F regions. Numbers above the bra
eighted characters. Numbers below branches i

ndi "i

Hy
-H
9,

solen wattii

Ар rotundifolia

Subgenus
Pentasepalae

Veronica m akowskiana
Veronica а
Subgenus

Ve nica persica Pocilla

Veronica amo опр
ons campylopoda

Veroni errata
Veronica a тип 1% А
nsis | Subgenus

Chamaedrys

e Ка раедегойейа)

Veronica O o oS
llos |
a

ubgenus
Stenocarpon
1 fe

Subgen
Pellidosperma

mple
js gulic.

ubgenus
Cochlidiosperma

gen
| iman
Subgenus Synthyris

e
Vero enus
ronica pere
Veronica Бе ДШ Beccabunga
Veronica ge lanoi es
inito Y |

a glandulosa African
spp.
Veronica m
E UND ap =
Subgenus
Veronica

Officinalis-
group

wulfenioid
grade

Veronica
Veronicastrum si igmonostach ys
Veronicastrum liukiuense

Globularia salicina

trees of the analysis of the combined data set of the

) y
e (Bremer support). CI = 0.47; RI = 0.70. Veronica

“bolkardaghensis” is an abbreviation for Veronica bombycina Ae bolkardaghensis.

Volume 91, Number 2
2004

Albach et al. 287

Evolution of Veroniceae

Oreosolen wattii

Lafuentea rotundifolia

Sibthorpia =

са

бе veronica

58 eronica
— — — ar

59 — Veronica o
| Veronica paederotae
veron ica bomb cina
eronica cuneifolia ,
— Veronica "bolkardaghensis Subgenus
88 Pentasepalae

ШШ

c бопса d

bi polita
Veronica persica Subgenus
— Veronica amoena Sei
Veronica campy opoda осша
Veronica ar [i -serrata

Veronica rubrifolia

99 Veronica arvensis | Subgenus

| Chamaedrys

Subgenus
rechti (Paederotella) Stenocarpon

li

со
55
©
3
o
Ф

S828

van uginos rwateri Hebe complex
ари yoides rap ane
it ubge

| | еи

Subgenus
| Cochlidiosperma

Subgenus Synthyris

Veronica
A

92

Subgenus
Beccabunga

ve ca
um pereg ina.
100 "CY Veronica ser lifoli
1901 lanoides
roni са Cini ja

Pseudolysimachium
African

|

'Veroniceae

| Officinalis-
group

Subgenus
Veronica

Bion‏ 1 بسا

a 7 kurrooa

wulfenioid
rade

nia ea inicum

0 - Veronicastrum stémonostachys
Veronicastrum liukiuense

Figure 4.

CT transitions in the ITS par N
equally weighted 8 ters; СІ =
bycina subsp. bolkardaghensis.

= аһо
‚42; RI = 0.69. Veronica

Globularia salicina

Strict ag "ini tree of 5000 most parsimonious trees of the analysis of the combined data set excluding

ve the branches indicate bootstrap percentages for the analysis of

“bolkardaghensis” is an abbreviation for Veronica bom-

288

Annals

of the
Missouri Botanical Garden

egsolen wattii
94 it a SIRO europaea

Veronica eroriak

a

eronica arvensis

verna
amaedrys
Ssa

ica”
s a
Il

ресі"

no

—
198— Veronica

Veronica

frúticy
ri

96

98

eronica trilo

ae
sularis

] А
Veronica heure
Veronica pere
eronica sorp [
eronica ge
Veronica Ол

бол
eronica

а=

98

Subgenus

фо ardaghensis Pentasepalae

gm akowskiana

Subgenus
Pocilla

| Subgenus
Chamaedrys
Subgenus
Stenocarpon
Hebe complex

тре
ronica 1 е Triangulic.

ы
5

Subgenus
Cochlidiosperma

Subgenus
Pseudolysimachium

100 — versie е B" Synthyris
nica

Subgenus
Beccabunga

Subgenus
Veronica

94

a
pane о mayor
а

Glo 78 ria. дЫ

Fig
likelihood prs sis

fuen ea Pu m

wulfenioid
grade

Ma ajor rity-rule consensus including all ci е groupings from 19,700 trees of the Bayesian maximum

. Numbers above the branches represe )ercent. recoveries

1 be translated as posterior

probabilities. Veronica * ‘bolkardaghensis” is an Kr M for Veronica bombycina “эш bolkardaghensis.

Volume 91, Number 2
2004

Albach et al.
аа of Veroniceae

ferences from other relationships suggested by the
analysis with CT transitions removed from the ITS
partition or supported by Bayesian maximum like-
lihood if necessary.

DISCUSSION

The combined analysis of ITS and trnL-F gives
us the most robust phylogeny of Veroniceae to date.
In the following, we will compare this phylogeny
with information about structural data, mainly from
the literature. This analysis is restricted to the most
important characters, due to space limitations. For
a more comprehensive discussion, the reader is re-
ferred to Albach (2002). Furthermore, the evolution
of the seeds will be discussed in a separate paper
(Martínez-Ortega & Albach, in prep.). While dis-
cussing these characters, we should be aware that
this phylogeny does not include all species and
therefore may be misleading. Our taxon sampling
was designed to minimize this effect but could not
exclude it completely. Additionally, the results of
the combined analysis are based on conflicting data
in the wulfenioid grade (see above). which may lead
to different inferences. We have discussed these
problems where necessary.

VEGETATIVE MORPHOLOCY

One of the main differences recognized in plant
morphology is whether the main shoot continues
growth (monopodium) or is substituted by a lateral
off-shoot in the next season (sympodium). Veroni-
ceae are variable in this character, and some spe-
cies do both. Mapping this character on one of our
most parsimonious trees (result not shown) shows
that strict monopodial growth is most likely ple-
siomorphic for Veroniceae and was subsequently
ost twice, once in Veronicastrum and once in the
clade formed by Paederota and Veronica. In Veron-
icastrum, Paederota, and most species of Veronica,
the shoot apex dies back after the flowering season
and new shoots arise from lateral buds in the lower.
vegetative region (Hamann, 1958). Within Veronica,
(V. officinalis. V. bec-

montana,

some species have been found (
cabunga, V. aphylla, V. V. cuneifolia, V.
filiformis, Hamann, 1958; V. caespitosa, V. bomby-
1969) that either re-

verted to monopodial growth, or kept it and the

cina, V. thessalica, Fischer,
terminal shoot continues to grow in the next season.
Possibly, even more are able to grow monopodially
but have not yet been investigated, e.g., East Asian
species of subgenus Veronica, such as V. pirolifor-
mis. Fischer (1969) hypothesized a phylogenetic
importance of prolification (innovation of a terminal

shoot normally discontinued). A comparison with

our phylogenetic hypothesis, however, does not
show prolificating species to be closely related. Pro-
lification is associated in Veronica with a plagiotro-
pous stature and the lack of a terminal inflores-
cence. The only exception is V. filiformis, which is
the only perennial member of the otherwise non-
prolificating annual subgenus Pocilla. All species
of this subgenus have a terminal inflorescence (see
The

development of a shoot from the terminal inflores-

discussion under inflorescence morphology).

cence in V. filiformis is, therefore, one possibility
to continue growth otherwise limited by a terminal
1942; 1951; Ha-

mann, 1958). In V. filiformis prolification may have

inflorescence (Lehmann, Thaler,
een the only possibility to continue growth, be-
cause the vegetative part had been reduced in its
annual ancestor and lateral buds were few or lack-
ing.

Pennell (1935) and Thieret (1955) arranged Ve-
roniceae in two series, one with cauline leaves and
the other with a basal rosette. Hong (1984) rejected
this arrangement, citing a correlation of alpine and
subalpine habitats with a basal rosette (see also
Körner, 1999). Species of Veronica subg. Synthyris
outside alpine regions may, therefore, have evolved
from more alpine ancestors from which they inher-
ited their rosette form. However, species of Veronica
subg. Synthyris and other species of Veronica differ
from other Veroniceae with basal rosettes, such as
Wulfenia,

stem and growing sympodially, whereas some spe-

in having the rosette on the flowering

cies of Veronica, Wulfenia, and also Plantago have
a terminal rosette with axillary inflorescences (mon-
opodium). It is noteworthy that Plantago, the in-
ferred sister to Veroniceae in several broad-scale
phylogenetic analyses of DNA sequence data (Olm-
stead & Reeves, 1995; Oxelman et al., 1999; Olm-
2000, 2001; Albach et al., 2001).

seems to have evolved from an ancestor growing

stead et al., also
monopodially with a basal rosette (Rahn, 1996). A
common origin of these basal rosettes, however, im-
plies that Aragoa, observed as sister to Plantago
(Bello et al., 2002), has lost its basal rosette. Within
the Officinalis group of subgenus Veronica, we have
a morphological transition series from a prolificat-
ing species (Veronica officinalis) via an intermediate
with a large shoot apex (V. grandiflora) to a rosette
species with a stunted shoot apex and pseudoter-
minal inflorescence (V. aphylla).

INFLORESCENCE MORPHOLOGY

The inflorescence morphology, especially the
presence or absence of a terminal inflorescence,
has been one of the main characters to divide Ve-

290 Annals of the
Missouri Botanical Garden

[Г Globularia salicina
Plantago coronopus

lten
Veronica ene

комга ca cuneifolia bgenus
Veronica 8 чый Pentasepalae

Veronica ‘bo on ‘
Veronica bom

Veronica оа
Veronica filiformis
Veronica agrestis
eronica polita
юа ре do Subgenus
eronica na Pocilla
[| Гераса campylopoda
Veronica argute-serrata

Subgen
од

гоп ет
Veronica ام ہنا‎
Veronica thes

a Veronic a ci hata Subgenus
eronica lanuginosa

Veronica rup chii pov Stenocarpon
veranos TN
Parahebe undo elen Hebe complex

Veroni са chamaepithyoides Subgenus Triangulicapsula
Veronica onii

ica don ubg
Veronica руй» `
ronica glauca ls
eronica crista-galli
Veronica panormitana Subae
Veronica frichadena u
eronica lycica
Veronica Hoppe Cochlidiosp pa
Veronica tril
[| E longifolia Subgenus
2 : ,
Veronica dahurica Pseudolysimachium

3 insularis Sub unu

eronica missurica

Veronica ре Deccapunge R
eronic

Veronica 5 Subgenus

Veronica serpyllifolia Beccabunga

Veronica gentianoides

Veronica acinifolia

v ronica morrisonicola | Subgenus
e A
Veronica allionii Veronica

Inflorescence

С] Terminal
ШШ only lateral
ШИШ solitary flowers
E] equivocal

Veronica copelandii
Veronica w wommskjoidii
ero

roi
Lagotis angustibracteata o
Lagotis stolonifera wulfenioid grade
Picrorhiza kurrooa
ё Wulfeniopsis fearing
AL) Veronicastrum virgin
Veronicastrum stemonostachys
Veronicastrum liukiuense
Figur rrence of a terminal inflorescence mapped on one most parsimonious tree from the combined analysis
(AC € TR AN a Veronica “bolkardaghensis” is an abbreviation for Veronica bombycina subsp. eres ae

ronica infragenerically in previous classifications rescence and that the presence of a terminal inflo-
(Rómpp, 1928; Elenevskij, 1977). We have dis- rescence has evolved at least five times, in
cussed earlier (Albach & Chase, 2001; Martínez- — Veronicastrum virginicum and relatives, in Paeder-
Ortega & Rico, 2001) that this character is more ota, in the Alpina group and in Veronica glandulosa
plastic than previously assumed. Mapping the pres- of subgenus Veronica, and in the remainder of Ve-
ence of a terminal inflorescence on one of our most ronica. In subgenus Veronica the character has
parsimonious trees (Fig. 6) indicates that the an- been apparently labile (Fig. 6), whereas it became
cestral condition is the absence of a terminal inflo- apparently more canalized in the rest of Veronica

Volume 91, Number 2
2004

Albach et al.
Evolution of Veroniceae

291

s.l. A different interpretation is possible consider-
ing that a terminal inflorescence is correlated with
1958; Albach et

al., in press a) and also often with alpine habitats.

an annual life history (Hamann,

Most of the alpine species with only lateral inflo-
rescences evolve a pseudoterminal condition (Fi-
scher, 1969; also in the montane V. urticifolia, Ha-
1958).

example, because these alpine dwarf plants have

mann, Veronica aragonensis is a good
typically pseudoterminal inflorescences, but plants
from lower altitudes have clearly axillary racemes
(Montserrat, 1968). In alpine species a seemingly
terminal inflorescence, which is derived either by
a truly terminal inflorescence or a pseudoterminal
inflorescence with a degenerated shoot apex, seems
to be favored by selection. A truly terminal inflo-
rescence may have evolved multiple times due to
selection pressure in these habitats from a proto-
Veronica and -Paederota with only lateral inflores-
cences. Following this argument, the transition from
the lack of a terminal inflorescence to its presence
is more likely than vice versa in the phylogenetic
history of Veronica, due to the repeated invasion of
alpine habitats and shifts to an annual life history.

Solitary flowers in the Agrestis group and sub-
genus Cochlidiosperma evolved in parallel. These
“solitary” flowers are subtended by leaf-like bracts
in contrast to a gradual change of leaf shape within
the inflorescence (e.g., V. tenuifolia Asso, V. ponae
Gouan) or scale-like bracts (e.g., V. glauca, V. spi-
cata) in other species. Hamann (1958), however,
concluded that the flower subtending leaves in the
Agrestis group and subgenus Cochlidiosperma are
foliaceous bracts, and these species do not have
This

was based on the observation that phyllotaxy in the

solitary flowers but terminal inflorescences.

inflorescence and the vegetative part of the plant
differ—opposite in the vegetative parts and alter-
nate in the inflorescence. Indeed, an ancestor with
a terminal inflorescence is inferred for both clades
with solitary flowers (Fig. 6), suggesting that in both
cases evolution proceeded toward enlarged bracts
compensating for reduced vegetative parts and
elongation of internodes in terminal inflorescences.

FLOWER DEVELOPMENT

The most obvious character of Veronica is its te-
tramerous short-tubed flower. However, despite sev-
eral descriptions of flower development in single
1883, for V. longifolia), com-
parative studies of flower development have been

species (e.g., Noll,

lacking. Only the study by Kampny and Dengler
(1997) provided comparable data for several spe-

serpyllifolia, V. lon-

cies (Veronica chamaedrys,

gifolia |= Pseudolysimachion longifolium], V. re-
gina-nivalis [= Synthyris reniformis], V. besseya |=
Besseya alpina]. the latter two from subgenus Syn-
thyris, Hebe parviflora (subg. Hebe), Derwentia per-
foliata (subg. Derwentia), Wulfenia carinthiaca, Ve-
ronicastrum virginicum, Digitalis grandiflora, and
Verbascum blattaria).

Stamens are initiated simultaneously with or be-
fore corolla initiation in all Veroniceae (Kampny &
Dengler, 1997). Development of the stamens is ini-
tiated before the corolla in the short-tubed flowers
1920).

is initiated at the same time as the corolla.

of the Veroniceae (Fischer, The gynoecium
This is
consistent with a delayed onset of corolla tube de-
velopment leading to its reduced size. Kampny e
Dengler (1997) found similarity in the speed о

flower part development of Veronica Ма
and subgenus Synthyris. For example, calyx lobe
growth is slowed just before anthesis. whereas its
growth is slowed at an earlier stage in the Hebe
complex. Calyx lobe growth is continuous in sub-
genus Pseudolysimachium and Veronica chamae-
drys, and decreases gradually in Veronicastrum. A
comparison of developmental timing also shows that
the tubular flower of Veronicastrum, V. longifolia,
and the Hebe complex developed differently, and
they are thus not homologous (Kampny et al., 1994;
Kampny & Dengler, 1997). Corolla tube growth ter-
minates just before anthesis in Veronicastrum,
whereas growth slows at an earlier stage in the
Hebe complex, probably because the mechanism
allowing corolla tube growth at a later stage was
lost in the short-tubed ancestors of the Hebe com-
plex. Flower development in Veroniceae is, as can
be seen from these examples. a mixture of hetero-
chronic events of increasing and decreasing speeds,
earlier and delayed onsets, and terminations of de-
1993).

heterochronic events is not restricted to a few long-

velopment (Kampny et al., This mixture of
tubed species but is also apparent in other species
of Veronica, in which relation of corolla tube to co-
rolla lobes is not identical but can vary from 2:5 to
1:8 (Aseyeva, 2002)

CALYX

In the calyx and corolla, reductions in the num-
ber of lobes from five to four have occurred. Reduc-

tions in the two kinds of whorls are not correlated
and therefore necessitate separate discussions. Re-
duction in calyx lobe number is due to loss of the
posterior lobe, whereas that in corolla lobes is due
to congenital fusion. Reduction in calyx lobe num-
ber characterizes Veronica s.l. Reversals to five ca-
lyx lobes, on the other hand, need to be hypothe-

292

Annals of the
Missouri Botanical Garden

sized for Veronica subsect. Austriacae (Wulff) Riek

‚ V. jacquinii, V. turrilliana), V. ruprechtii Me-
derovella), * and some other isolated
species in subgenera Veronica, Pentasepalae, Sten-
ocarpon, and the Hebe complex. However, the pen-
tasepalous flower is not constant within species

‘Chionohebe”

(even within individuals!) of Veronica subsect. Aus-
triacae, nor is the tetrasepalous flower constant in
the remaining species (Lehmann, 1918). Further-
more, there is a distinction in the pentasepalous
state of Veronicastrum and Veronica subsect. Aus-
triacae, because in the former the posterior sepal
is formed as the third sepal and well before the
corolla, whereas in the latter it is formed after the
corolla (Fischer, 1920). There is some variation in
the formation of front and back sepals (Fischer,
1920), but sufficient data to allow any inference are
lacking. Further investigation into the development
of the calyx in Veroniceae and Plantago seems nec-
essary to test the homology of tetramerous calyces
in the two groups. Investigations up to now indicate
non-homology due to the loss of the fifth sepal in
Veroniceae and, in contrast, fusion of two lobes into
the ventral lobe in Plantago lanceolata (Hender-
1920).

son,

COROLLA

Apart from the reduction in calyx lobe number,
we also find a reduction in number of corolla lobes
from five to four. Whereas the reduction in calyx
lobe number is not stable, the tetrapetalous flower
in Veronica is rather = (Lehmann, 1918). F
ceptions occur in (subg. Synthyris)
where the corolla is lost, and V. ruprechtii ( = Pae-
derotella pontica; probably subg. Stenocarpon),
“Detzneria,” and “Chionohebe” (subg. Hebe) with
pentapetalous corollas. However, corolla lobe num-

esseya"

ber can vary between two and eight within individ-
uals and populations in a few species (like V. fru-
ticans), sometimes remarkably frequently (pers.
obs.). A pentamerous (and tetraploid) form of V. er-
inoides has been the basis of a new species (Con-
tandriopoulos & Quézel, 1964), though it is prob-
ably nothing more than an aberrant, teratological
small population (according to Fischer, 1991). Т

ditionally, a pentamerous corolla has been overrat-
ed as a diagnostic character in Veronica. Outside
Veronica, the tetrapetalous corolla occurs in Picro-
rhiza scrophulariiflora, Veronicastrum, Scrofella,
Wulfeniopsis, and Paederota. Lagotis is extremely
variable in this respect, having most commonly
three corolla lobes. Mapping this character on the
molecular tree (result not shown) implies a tetram-
erous corolla in the ancestor of Veroniceae and re-

versals in Picrorhiza kurrooa, Wulfenia (and Kash-
miria), some African of Veronica, V.
ruprechtii, “Detzneria,”
ter-group relationship of Veroniceae and the tetram-
erous Plantago hypothesized in most analyses of
molecular data sets (Olmstead & Reeves, 1995; Ox-
elman et al., 1999; Olmstead et al., 2000, 2001;
Albach et al., 2001) and the sister-group relation-
ship of Aragoa and Plantago (Bello et al., 2002)
indicated that tetramery may be plesiomorphic in
the clade of Plantago and Veronica. Reeves and
Olmstead (1998) first speculated about a common
origin but emphasized the need for increased taxon

species
and *Chionohebe." The sis-

sampling. With the increased taxon sampling here,
we still infer the common origin of a tetramerous
corolla in the clade of Plantago, Aragoa, and Ve-
roniceae if Digitalis and Erinus are sister to this
clade. However, there might also have been just a
tendency for corolla lobes to fuse in the earliest
species of Plantago and Veroniceae; these species
could then have been the ancestors of multiple spe-
cies with tetramerous corollas. Thus, a predisposi-
tion to form tetramerous flowers would be a syna-
pomorphy for the clade containing Plantago and
Veroniceae.

The fusion of corolla lobes in Veronica involved
the two adaxial corolla lobes. This fusion is more
r less complete, with some corollas still showing

a notch in the adaxial corolla lobe. In those flowers
without a notch we may still find two nerves in the
one adaxial corolla lobe as a relic of the two sep-
arate lobes, whereas in others fusion is more com-
plete and only one nerve is present (Lehmann,
1918). Vascular patterns were studied in detail by
Saunders (1934), who showed that the reduction
from five corolla lobes to four preceded the reduc-
tion from two to one midrib in the adaxial lobe
derived from the fusion, and that the reduction to
one midrib was incompatible with the occurrence
of a fifth sepal. A comparison with the classification
of that time gave a confusing picture of multiple

) A

parallel evolutionary trends (Saunders, 19:

comparison of the data from Saunders (1934), to-
gether with additional information by Aseyeva
2002) and our molecular hypothesis, however,
gives a much clearer picture (Fig. 7). The reduction
to a single midrib is strictly confined to three
subgenus

—

clades—subgenus | Pseudolysimachium,
Beccabunga, and subgenera Cochlidiosperma plus
Pellidosperma (but not in V. crista-galli), although
Aseyeva (2002) reported a single midrib also from
V. biloba (subg. Pocilla, not sampled in our analy-
sis). The most parsimonious interpretation is then
a reversal in the clade of subgenera Pentasepalae,

Pocilla, Chamaedrys, Stenocarpon, Derwentia, and

Volume 91, Number 2 Albach et al. 293
2004 Evolution of Veroniceae

Plant
Planta

Veronica oltensis

Veronica paederotae

Veronica cuneifolia Subgenus
eronica jacquinii

Veronica fumlliiana T Pentasepalae

Veronica ‘bolkardaghensis

Veronica bombycina
eronica czerniakowskiana

Veronica filiformis

Veronica agrestis

ca

Veroni l

Veronica persica Subgenus
Veronica amoena ocilla
Veronica campylopoda

Veronica argute-serrata

Veronica rubrifolia

Veronica arvensis Subgenus

Veronica vema

Veronica chamaedrys Chamaedrys
Veronica thessalica

Veronica ciliata. Subgenus
Veronica lanuginosa Stenoca rpon

Veronica ruprechtii (Paederotella)
Veronica fruticulosa
Parahebe vanderwateri Hebe complex |

Veronica chamaepithyoides Subgenus Triangulicapsula
Veronica donii baenús

Veronica triphyllos u :
eronica Pellidosperma

Veronica trichadena Subgenus
C

eronica lycica idi

Veronica sublobata Cochlidiosp erma
veronica 8 "

eronica longifolia
Veronica spicata Subge

nus
Veronica далса Pseudolysimachium
Veronica missurica - Subgenus Synthyris
ronica heureka

na Subgenus
Veronica serpyllifolia Beccabunga
S

Veronica vandellioides
Veronica morrisonicola Subgenus
Veronica allionii Veronica

Veronica aphylla
Veronica bellidioides
a

La -
Lagotis stolonifera wulfenioid grade

Number of veins in corolla

[— ] Five veins Veronicastrum liukiuense
ШШ Four veins
Figu Occurrence of four and five corolla veins mapped on one most parsimonious tree from the combined
analvsis (ACCTRAN optimization). Only species names with character state boxes in front of the name have been
studied. Veronica "bolkardaghensis" is an abbreviation for Veronica bombycina subsp. bolkardaghensis.

re i.

Hebe. However. the re-emergence of the second Flower size is also not a phylogenetically stable
midrib in the posterior corolla lobe after it has been character, with size varying considerably between
lost once seems unlikely. Therefore, the possibility closely related species. For example, Veronica ver-
of a parallel evolutionary shift to a single midrib ла and И chamaedrys, V. triphyllos and V. donit or
should be considered. Further analyses on the vas- V. panormitana/V. trichadena and V. lycica are sis-

—

cular pattern in species not investigated so far and pairs in our analysis (Figs. 1—5) that differ
on the correlation of the fifth calyx lobe and the grossly in flower size, with the first in these pairs

lack of fusion in midribs would be worthwhile. having a minute flower and the second having a
© D

Annals of the
Missouri Botanical Garden

flower three to four times the size. Reduction in
flower size is probably in all these cases due to a
shift to a selfing breeding system.

Flower color is often not even stable within spe-
cies. Flowers are mostly variations of white, pink,
purple, or blue with the exceptions of Paederota
lutea, тее integra, Veronicastrum brunonianum,
and V. formosanum, which have yellow corollas.
Additionally, flower color is often variable within a
species, with a tendency for alpine varieties to have
darker blue corollas. Blue flowers are warmer than
white flowers (Savile, 1972) and are therefore more
attractive for pollinators.

PALYNOLOGY

Pollen offers a variety of characters that have
been used for taxonomic purposes in Veroniceae.
Hong (1984) intensively studied pollen morphology
within Veroniceae and recognized eight different
types. By comparing his results with our phyloge-
netic hypothesis, some evolutionary trends of pollen
grain characters can be revealed. The type of pollen
of Plantago and Aragoa is completely different
from that of Digitalis and Veroniceae and is there-
fore an autapomorphy (Bello et al., 2002). Digitalis
has three-colporate, isopolar-spheroid pollen with a
wide colpus and microreticulate tectum (Minkin &
Eshbaugh, 1989). This type of pollen resembles
that of Hong's Paederota type, which occurs in Pae-
derota, Wulfenia, Lagotis, Picrorhiza scrophulari-
iflora, and subgenus Pseudolysimachium of Veron-
ica (Hong, 1984; Argue, 1995). It is inferred to be
ancestral in Veroniceae (result not shown) and ple-
siomorphic in Scrophulariaceae (Argue, 1995).
From this, we can infer the derivation of Hong’s
Scrofella type in Scrofella, Veronicastrum, and Pic-
rorhiza kurrooa and his Wulfeniopsis type in Wul-
feniopsis by assuming a narrowing of the colpus,
elongation of the os (indistinct in Wulfeniopsis), and
perforation and smoothing of the tectum. The first
two characters may be correlated with the decrease
in size (especially a narrowing from a spheroid form
to a prolate form) in these two types. Apparently
the Scrofella type evolved twice in Veronicastrum
and Picrorhiza kurrooa or the Paederota type re-
evolved in P. scrophulariiflora. However, we should
be careful with this inference, because relation-
ships in the wulfenioid grade are only weakly sup-
ported. Assuming the relationships in the ITS anal-
ysis (Fig. 1) are correct, as supported by Bayesian
maximum likelihood analysis of the combined data
set (Fig. 5), would require an independent origin of
the Scrofella type pollen in Veronicastrum and the
Picrorhiza-Wulfeniopsis clade.

The distinction between these three types and
the remaining five types coincides with the distinc-
tion between Veronica s.l. and the wulfenioid grade.
It is marked by the change from a three-colporate
to three-colpate pollen. The function of pores in the
colpi is unclear, but their loss may be associated
with prevention of water loss. Other differences in-
clude the microreticulate tectum in the Paederota
type versus a striate-reticulate tectum in Veronica.
Exceptions to this distinction are V. javanica, V. oli-
gosperma (Huang, 1972), and subgenus Pseudoly-
simachium, which
(Hong, 1984). Veronica schmidtiana from subgenus

Pseudolysimachium constitutes an exception from
the exception with having Veronica type pollen
(Hong, 1984). Thus, the three-colporate pollen in
Pseudolysimachium may be a reversal. More de-
tailed investigation of relationships and pollen evo-
lution within this group is necessary. Hong (1984)
recognized two main types among species of Veron-
ica, his Veronica and Stenocarpon types. However,
he noticed intermediate species between these two
similar types, which was later confirmed by a more
detailed analysis (Martínez-Ortega et al., .
They suggested multiple origins of Hong's Steno-
carpon type (with tectum neither typically micro-
nor typically striate-reticulate) from his Veronica
type (with striate-reticulate tectum), which is sup-
ported by a comparison with our phylogenetic hy-
pothesis (result not shown). Within Veronica, Mar-
tinez-Ortega et al. (2000: 27) found “the value of
pollen characters as taxonomic tools. . .restricted to
a small number of cases and does not seem very
remarkable." One of these cases is the clade of
subgenera Pellidosperma and Cochlidiosperma,
which share a perforate tectum, a narrow colpus
with jagged margins, and a more oblate shape
(Hong, 1984; Fernández & Pastor, 1997). Within
this group, pollen of V. crista-galli is differentiated
by an irregularly rugulose tectum, whereas the re-
mainder of the subgenus has supratectal spinules
(Hong, 1984). The pollen of V. crista-galli is
thought to be a specialized form of the Stenocarpon
type, whereas the pollen of subgenus Cochlidios-
perma does not resemble any other Veronica pollen
Hong & Nilsson, 1983; Hong, 1984). Based on
these differences in pollen, together with smaller
differences in other characters, Hong and Nilsson
(1983) re-erected the genus Cochlidiosperma
(Rchb.) Rchb. for subgenus Cochlidiosperma with-
out V. crista-galli and аа for V. crista-
galli and V. simensis. The last pollen type recog-
nized by Hong (1984) is Erst de by Detzneria
tubata only, a species divergent in many respects,
including having larger pollen with oblong lumina,

—

Volume 91, Number 2
2004

Albach et al.
Evolution of Veroniceae

a smooth colpus membrane, and a macroreticulate
tectum (Hong, 19

CAPSULE

According to Hong (1984), capsules of Veronica
are characteristically laterally compressed and two-
lobed in contrast to the turgid, apically e
capsules of the wulfenioid grade. He outlined :
simple progression from turgid and apically pins

capsules via the apically tapered but compressed
capsules (e.g., И eriogyne) to the increasingly com-
pressed and two-lobed capsules. This hypothesis is
one of the reasons why cladograms by Hong (1984)
(1997) show a sister-
group relationship of the Hebe complex and other

and Kampny and Dengler
subclades of Veronica. This simple evolutionary
trend is not compatible with our hypothesis based
on DNA sequence data (comparison not shown).
Compressed, wide capsules are probably synapo-
morphic for Veronica s.l., but then several different
trends occurred. Specializations led to loss of half
the capsule, megaspermy (all species of subg.
Cochlidiosperma), and globose capsules in subge-
nus Cochlidiosperma (all species except V. crista-
galli). Flabellate or rhombic capsules evolved
the series Canae of subgenus Veronica, and obdel-
tate capsules in subgenus Triangulicapsula. The
separation of the two capsule halves is taken to the
extreme in the relationship of V. biloba. In subge-
nus Pseudolysimachium, capsules either retained
an ancestrally thicker capsule or regained the ovoid
capsule. Tendencies to a longer and less wide cap-
sule, which is correlated with a less emarginate and
two-lobed condition, occurred in parallel in the Of-
ficinalis- Alpina group of subgenus Veronica and in
V. anagallis-V. aquatica and relatives. The greatest
diversity in capsule shape is found subgenus
Stenocarpon. Here, capsule shape varies from cor-
date (V. thessalica, V. saturejoides), to suborbicular
to widely elliptic (V. fruticulosa, V. mampodrensis),
to orbicular (V. ruprechtii), to oblong-lanceolate (V.
fruticans, V. ciliata). The fruit apex .
varies between notched, obtuse, and acu

Within the Hebe complex, capsule bin Was
used to differentiate Parahebe species with laterally
compressed, apically notched capsules from Hebe
species with dorsiventrally compressed, apically ta-
pered capsules (van Royen, 1972). However, the
clear distinction did not hold in New Zealand, al-
though DNA sequence analysis showed that those
species of subgenus Hebe with laterally ж d
capsules (e.g.. Hebe “Semiflagriformes” and “Gran-
diflorae”; Moore € Ashwin in Allan, 1961) fall into
the grade at the base of the main Hebe clade to-

gether with species of “Parahebe” (Wagstaff € Gar-
nock-Jones, 1998). We can, therefore, be sure that
the ancestor of the Hebe complex had a laterally
compressed capsule, and the dorsiventrally com-
pressed capsule probably arose only once.
Capsule dehiscence is an important character in
Veroniceae, representing important steps in their
evolution. The combination of a septicidal and loc-
ulicidal dehiscence is a synapomorphy for the tribe
because other Scrophulariaceae have mostly septi-
cidal capsules (Kampny & Dengler, 1997). Within
Veronica s.l., dehiscence is correlated with capsule
morphology. In species with cordate capsules, the
opening is loculicidal, whereas in species with an
apically tapering capsule the opening is generally

—

oculicidal and septicidal. This septicidal opening
differs, however, from the usual mode because the
median column remains intact, whereas in true sep-
ticidal openings the median column is also parted
(Rómpp. 1928).

Capsule dehiscence used to be cited as diagnos-
tic for Veronica s. str., with а loculicidal capsule,
and species of the Hebe complex, in which the cap-
sule is pseudo-septicidal and only to some extent
1972). However, sev-

eral Veronica species, such as V. javanica, V. fruti-

loculicidal (e.g.. van Royen,
culosa, subgenus Beccabunga, subgenus Pseudol y-

simachium, and some species of subgenus
Pentasepalae also are partly pseudo-septicidal by
means of a median fissure (Rómpp. 1928) to semi-
septicidal with an apical rupture of the placentar

column (MMO, pers. obs.)

EMBRYOLOGY

Endosperm formation, especially the formation of
chalazal and micropylar endosperm haustoria, were
studied by Gscheidle (1924), Weiß (1932), Glisic
1937), Yamazaki (1957), and Afanasiyeva (1971).
Glisic (1937) gave a first phylogenetic scheme for

—

the evolution of the endosperm in Veroniceae,
which is shown in Figure 8. The only members of
Veroniceae outside that have been
studied are Wulfenia and Veronicastrum (Gscheidle,
1924; Wei. 1932: Yamazaki, 1957). Both are char-
acterized by a uninucleate four-celled chalazal and

Veronica s.l.

a uninucleate four-celled (later a four-nucleate one-
celled) micropylar haustorium (Weiß, 1932; Yama-
zaki, 1957; Veronica | sensu Glisic, 1937, Fig. 8).
Species of subgenus Pseudolysimachium have the
same type of endosperm formation, which is be-
lieved to be primitive in Veroniceae (WeiB, 1932;
Glisic, 1937; 1957,
Glisic, Fig. 8) and occurs outside Veroniceae in

Erinus and Digitalis (Glisic, 1937; Hartl, 1966).

Yamazaki, Veronica ЇЇ sensu

Annals of the
Missouri Botanical Garden

0
LÀ
€

ejo v

— 7
x ¡o NY e
Veronica ied e Neronica V b
I 1

С

Veronica V1

Figure 8. Phylogenetic scheme of endosperm evolu-
tion in Veronica, modified from Glisic (1937). The chalazal
region is on the top of the embryo, the micropylar region
on the bottom.

Glisic’s scheme (1937, Fig. 8) fits nicely with our
molecular hypothesis in showing a trend of reduc-
tion from the primitive type discussed above to an
intermediate type that differs in having only a two-
celled chalazal and a binucleate two-celled micro-
pylar haustorium. It can be found in species of the
Alpina and Officinalis groups in subgenus Veronica
(Gscheidle, 1924; Weiß, 1932; Yamazaki, 1957;
Afanasiyeva, 1971; Veronica IV. V sensu Glisic,
1937, Fig. 8). It can also be found in V. scutellata,
V. fruticulosa, and V. austriaca (Afanasiyeva, 1971).
The latter result is surprising and needs confirma-
tion, because all related species show a different

endosperm development (see below). The African
group of subgenus Veronica has not been studied
Two other species from subgenus Veronica, V.

montana (Afanasiyeva, 1971) and И miqueliana
(Yamazaki, 1957), differ from the previous species
in having only one cell in the chalazal haustorium,
which is, however, binucleate. This is the chalaza
haustorium type found in most species of Veronica
(incl. Hebe; Gscheidle, 1924; WeiB, 1932; Yama-
zaki, 1957; Afanasiyeva, 1971, Alectorolophus-
type sensu Glisic, 1937, Fig. 8). Chalazal haustoria
from species of the subgenera Pentasepalae and
Chamaedrys share the distinctive feature of a lat-
eral appendage (Weiß, 1932; Yamazaki, 1957). This
appendage was also found in V. persica by Yamazaki
(1957) but not by Gscheidle (1924) and Weiß
(1932). The micropylar haustorium also experienc-
es a reduction in some taxa. In species from sub-
genus Cochlidiosperma (but not V. crista-galli) and
V. miqueliana the micropylar haustorium consists
of two uninucleate cells in contrast to the two bi-
nucleate cells in other species of Veronica (Yama-
zaki, 1957; Afanasiyeva, 1971, Veronica VI sensu
Glisic, 1937, Fig. 8). Other than this reduction in
nuclei number, the micropylar haustorium is vari-
able in overall shape but lacks diagnostic charac-
ters for the distinction of different types over the
whole genus (Gscheidle, 1924; Weiß, 1932). Var
ations characterizing smaller groups of species are,
however, possible, such as the more aggressively
invading haustorium of the Beccabunga group (in-
cluding V. peregrina) in comparison with the Ser-
pyllifolia group. Thus, endosperm development in
Veronica shows an increasing reduction in number
of cells and nuclei, which is more primitive and
labile in the first-branching clades of Veronica and
becomes more canalized subsequently and leads to
the most reduced stage in subgenus Cochlidiosper-

ma.

CHROMOSOME NUMBER

Chromosome numbers are available for many
species of the Veroniceae. By mapping chromosome
numbers on our phylogenetic tree (results not
shown) we can infer some trends regarding the kar-
yological evolution. However, no answer can be giv-
en to the question about the ancestral number of
chromosomes. Lepper (1964) hypothesized an an-
cestral number of x — 5 followed by a polyploid
event and subsequent reductions. Outgroup com-
parison is inconclusive, with three different base
numbers found in our outgroups, x — 8 in Globu-
laria, x = 7 in Digitalis and Erinus, and x = 6 as
the ancestral base number of Plantago hypothe-

Volume 91, Number 2
2004

Albach et al. 297
Ead of Veroniceae
ebe ман
afue niea Е folia
Subgenus
Pentasepalae
NI Subgenus
Veronica am Pocilla
— Veronica RD a
ond 5 доба
Мег arguté-serrata
| Subgenus
Chamaedrys
A Subgenus
Seo (Peedorotela) Stenocarpon
a,

ebe complex
yu riahgulic.

ubgen
5
bgenus
a Cochlidiosperma
M T i ola
38b 13 25 42f Zr 198 Ѕирдепиѕ
rmm D ا‎ ca hi

ы: oua rd ا‎ dre E Pseudolysimachium
4 ] ] .
| Mi — Veronica missurica Subgenus Synthyris
Veronica | 1 —V a
19

313 АШ Veronica eureka Subgenus
“Ый 27 356 Veronica реп 69% ffo Beccabunga
2433 4? Ly y оша a genta ili olia

Officinalis- Subgenus
group Veronica

a aphylla
po ee -Veronica bellidioides
| а M Ce — Veronica шс Wa, Alpina-
veronica copelandii
zB "e Ve ronica ар А skjoldii | STOP
4 —Ю% ronica
238 || FR
8

8 (variable)
2 a

[Ба
T mM
| аппаса wulfenioid
m~ Lagotis angustibracteata
10ba 18,2 onifera grade
12 18a рге /
E Шш u

7 4 1. —
Veroniceae ея

Veronicasirum d Z

* [2A 2199 т
А = B DM es
-p Ml "€ Planta о lanceolata

i s HA salicina
9

ure Structural, ecological, and phytochemical synapomorphies as discussed in the text mapped onto one most
parsimonious tree from the combined analysis

. Parallel bars refer to parallelisms, gray boxes to rar ашы аш s with
eversals, and black boxes to synapomorphies Бо reversals. The numbers match those in Table

298 Annals of the
Missouri Botanical Garden

Table 2. Characters of Veroniceae and their states that are possible synapomorphies for various taxa in the tribe.
See Figure 9 for details of their distribution.

Character # Character Derived character state
1 habitat aquatic habitat (see Albach, 2002)
2 growth form basal rosette
3 indumentum loss of eglandular hairs (see Albach, 2002)
4 hair type branched hairs en Albach, 2002)
5 flower organization solitary flowe
6 flower development stamen initiation simultaneously or before corolla initiati
7 calyx calyx lobe reduction to four; if five, last sepal formed de corolla
8 corolla a—tetramerous corolla
b—pentamerous corolla
9 corolla venation a—four petal veins
b—five petal veins
10 androecium a—two stamina
b—four stamina (see Albach, 2002)
11 androecium ridged anther cells (see Kampny & Dengler, 1997)
12 pollen structure narrowing of the colpus, CAMAS of the os (indistinct in Wulfeniop-
sis), e of tectu
13 pollen structure a—three-colpate pollen
b—three-colporate pollen
14 pollen structure striate-reticulate pollen
15 ollen structure perforate tectum, narrow colpus with jagged margin
16 pollen structure rugulose tectum
17 pollen structure supatectual spinules
18 stigma a—reduced stigma
b—no reduced stigma (see Albach, 2002)
19 fruit morphology laterally compressed capsule
20 fruit morphology globose capsules
21 gynoecium reduction of ovule number per locule to one
22 fruit morphology triangular capsules
23 fruit morphology septicidal and loculicidal capsule opening
24 seed dispersal hygrochasy (see Albach, 2002)
25 embryology a—four-celled en

b—one- or two-celled haustoria
c—uni-nucleate two-celled micropylar haustorium
d—two-celled chalazal haustorium

l

26 embryology lateral haustorium appendage

27 embryology aggressive endosperm haustorium

28 gynoecium anatropous ovule (see Albach, 2002)

29 seed morphology flattened seeds (see Albach, 2002)

30 seed morphology cyathiform seeds (see Albach, 2002)

31 seed morphology seeds flatter than 0.2 mm (see Albach, 2002)

32 seed morphology cohlidiospermous seeds, larger than 2 mm si Albach, 2002)
33 seed morphology seeds less than 0.02 mg (see Albach, 2

34 seed number more than 30 seeds 15 capsule (see c h, 2002)

35 seed ultrastructure a—verrucate seed c

b—colliculate seed « coat
c—reticulate-corrugate seed coat

d—alveolate seed coat (see Albach, 2002)
36 seed ultrastructure regularly thickened radial walls (see Albach, 2002)
37 seed morphology endosperm podium with cork plate (see Albach, 2002)
38 seed ultrastructure a—no seed coat

b—intermediate layer of integument participates in seed coat (see Al-
bach, 2002
39 seed ultrastructure a—corky outer integument layer

b—papillae on outer integument layer

c—cellulose lacking in outer integument layer (see Albach, 2002)

Volume 91, Number 2 Albach et al. 299
2004 Evolution of Veroniceae
Table 2. Continued.
Character # Character Derived character state
40 аиа mussaenoside (see Albach, 2002)
41 phytochemis 8-OH-flavones (see Albach, 2002)
42 chromosome cies a—x
b=x = 7
C—x 6
d—x = 11
e—x = 12
х = 17
х = 2]
43 protein bodies in the nu- ‘leus
cleus 5 like protein hus in nucleus (see Albach, 2002)
sized by Rahn (1996). Species of the wulfenioid in subgenus Beccabunga. Two of its three sub-

grade are heterogeneous with respect to their chro-
mosome base number. All species of Veronicastrum
and Picrorhiza have x = 17, and x =
all species of Lagotis studied so far. Wulfeniopsis
has x = 8, whereas Wulfenia has x = 9 as do many
species of Veronica, although Lepper (1964) doubt-
ed the homology of these chromosome numbers
based on differences in chromosome morphology.
The result of x =
ber of Veronica is in contrast to the hypothesized
ancestral base chromosome number x = 8

9 as ancestral chromosome num-

eh-
mann (1940). This latter number has apparently
evolved just once in the clade consisting of sub-
genera Pentasepalae, Stenocarpon, Chamaedrys,
Triangulicapsula, Pocilla plus the Hebe complex.
However, chromosome number evolution continued
to x = 7 in subgenus Pocilla, x = 6 in subgenus
Triangulicapsula, and x = 21 in the Hebe complex
(with subsequent reductions to x = 19 and x = 20
see Wagstaff & Garnock-Jones, 1998).

Whereas the base chromosome number of x = 8
has apparently evolved just once, x = has
evolved at least three times independently in Ve-
ronica (Albach & Chase, 2001). A fourth incidence
(not included here) would be V. baumgartenii, a
relative of V. aphylla in subgenus Veronica. In the
first three incidents inferred here, the aneuploid
reduction to x =

»

7 is associated with a switch to
an annual life history. This kind of aneuploid re-
duction in chromosome number is also known from
other annuals (Stebbins, 1958; Raven, 1979). In
subgenus Pocilla, all species are annuals and have
x = 7. In subgenus Pellidosperma, the base number
reduction evolved after the evolution of the annual
life history in V. triphyllos, but V. praecox, a member
of subgenus Pellidosperma not sampled here, has
the inferred ancestral character state of x —
contrast, base number reduction seems to have
evolved before the switch to an annual life history

groups (the Acinifolia and Serpyllifolia groups)
have x — 7, whereas the remaining species have x
— 9. However. only the Acinifolia group consists
of annual species.

A reduction in base chromosome number (dys-
ploidy) among annual species relative to their pe-
rennial progenitors has been shown in other groups
of plants (e.g., Arabidopsis thaliana: Koch et al.

; Asteraceae: Babcock, 1947; Jackson. 1962:
Watanabe et al., 1999; Baldwin et al. 2002;
Dipsacaceae: Ehrendorfer, 1965). Reduced chro-
mosome number, however, is only one aspect of an-
nuals to reduce the recombination rate (Ehrendor-
fer, 1970). Another common trend is the evolution
of selfing. Recombination may be a disadvantage in
annuals because maintaining successful combina-
tions of genes is more important than in perennials,
which can compensate for low hybrid-pollen and
-seed fertility by reproducing again in the following
year (Stebbins, 1950). Therefore, increased linkage
of genes seems favorable in annuals. This linkage
seems connected with more temporary habitats
(Stebbins, 1958). In line with this argument, those
annual Veronica species living in the most mesic,
stable habitats (subg. . retained the
high base chromosome number o "he rea-
son for this connection, however, is not completely
clear, but it may be due to the fact that smaller
population sizes in unstable, ephemeral habitats al-
low faster fixation of mutations and contain less ge-
netic diversity, which may be advantageous in out-
breeding events. A second non-exclusive
hypothesis is that recombination as a defense
against pathogens is not necessary because of the
short life-span and less pathogen pressure in
ephemeral and xeric habitats (Watanabe et al.

The strange chromosome number of Veronica per-
egrina, with 2n = 52, and its annual habit have

300

Annals of the
Missouri Botanical Garden

confused many systematists. Our molecular analy-
ses (Albach & Chase, 2001;

position within the mi group with a base

1—5) revealed a
chromosome number of x — 9. Therefore, V. pere-
grina seems lo be a hexaploid member of this
group, which subsequently lost two chromosomes.
Supporting this view is the occurrence of two or
three particularly large chromosomes in V. peregri-
na (Hofelich, 1935), which may be the result of
Robertsonian fusion. Another example of reduced
chromosome number after a polyploid event is sub-
genus Pseudolysimachium with x = Afanasi-
yeva and Meshkova (1961) hypothesized an origin
from one parent with x — 8 and the other with x
— 9, whereas Graze (1935) assumed an origin from
an ancestor with x — 18 derived from diploid par-
ents with x — 9, based on a larger chromosome in

species of subgenus Pseudolysimachium with n =
17 and two larger chromosomes in those with n =
34. Additionally, Graze (1935) reported the occur-
rence of a variety of И longifolia with 36 chromo-
somes of equal size. Given the congruent results
from both the nuclear genome (Albach & Chase,
2001; Fig. 1) and plastid genome (Albach et al., in
Fig. 2) that place subgenus Pseudolysi-
machium among the subgenera with x — 9 and dis-

press а;

tant to subgenera with x = 8, Graze's hypothesis
seems more plausible.

CONCLUSION

Veronica is an example of reduction of parts in
various characters. As shown for the fifth stamen in
Lamiales (Walker-Larsen & Harder, 2000), the re-
duction of parts is reversible among taxa branching
from basal nodes and less so among derived taxa.
This indicates increased canalization of characters
in these derived taxa in which mutations leading to
reversal are becoming less and less probable be-
cause of subsequent mutations. The reason the re-
duction in parts is so common in Veroniceae may
Lehmann, 1918).

In flowers, adaptation to other pollinators that pre-

be correlation of characters (e.g..

fer short and rotate corolla tubes may have neces-
sitated the reduction of many parts, starting a cas-
cade of subsequent mutations in other parts of the
flower. The same may be true for the evolution of
annual species that experienced parallel reductions
in stature and phytochemical arsenal (Albach et al.,
in press a; Taskova & Albach, in prep.). Parallel
evolution makes it difficult to find synapomorphies
for all clades. We have mapped those discovered in
this study on one of our most parsimonious trees
from the combined analysis (Fig. 9 for ecological,
structural, and phytochemical characters). Compar-

ison of Figure 3 and Figure 9 shows a general cor-

relation of molecular and structural evolution.
Clades well supported by nucleotide characters
tend to have more structural synapomorphies. Fur-
thermore, evolutionarily stable characters can be
found in every kind of structure and developmental
process—seed, embryo, pollen, corolla, and flower
development. However, many of these characters
are difficult to observe and are therefore not useful
to identify subgenera in the field. This study further
stresses the need for more information on structural
characters to understand the evolution of our study
group.

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CLADISTIC RELATIONSHIPS
OF AECHMEA
(BROMELIACEAE,
BROMELIOIDEAE) AND
ALLIED GENERA!

Ana Paula Gelli de Faria,? Тата
Wendt,? and Gregory К. Brown?

ABSTRACT

Aechmea (ca. 220 species) is the largest and most diverse genus in Bromelioideae (Bromeliaceae), and s

veral

dissimilar generic concepts and infrageneric classifications have been proposed, frequently involving other Ke dy

related Bromelioideae. A morphology-based phylogenetic analysis using pars
subger nera represented) and. 34 exemplars from 9 closely an d genera as
Two species of C ryptanthus were included as the outgroup. '

imony was conducted with 86 taxa, in-

e main objectives were to assess the validity

of the major infrageneric classification systems proposed for Aechmea and to elucidate the phylogenetic position of

Aechmea and putatively related genera in subfamily Bromelioideae. The topology of the consensus tree
n-Brazilian Ronnbergia may be 5 Hohenbergia, Streptocalyx, and
eti " as are most subgenera of A

Characters. traditionally emphasized in

suggests thal

Aechmea, except for subgenera Chevaliera and

classifications of Bromelioideae

displayed mw levels of фиш зу, апа this may be a reason for the artificiality of the taxonomic systems proposed

for these taxa. Due to weak i
results do
for Le studies.

words:

ernal support, we refrain from recognizing any new taxonomic rearrangements. These
provide new А into the relationships within a number of Bromelioideae genera and suggest directions

Aechmea, Bromeliaceae, Bromelioideae, morphology, phylogeny.

In the most recent monograph for Bromeliaceae
Smith and Downs (1974, 1977, 1979) placed 2110
species in 48 genera and 3 subfamilies: Pitcair-
nioideae (740 spp.. 15 genera) Tillandsioideae
(806 spp., 6 genera), and Bromelioideae (564 spp.,
27 genera). During the past 20 years nearly 1160
additional species have been described, d
the family by half to ca. 3270 species and 5 -
era (Luther & Sieff, 1994, 1997; Luther, Pon
2001)

Aechmea Ruiz & Pav. (ca. 220 species; Luther,
2000) is the largest and most diverse genus in Bro-
melioideae with a distribution throughout tropical
America. Nearly 70% of Aechmea species (Smith
& Downs, 1979; Luther & Sieff, 1994, 1997; Lu-
ther, 2001) are distributed in Brazil, and the At-
^n Rain Forest is the center of diversity for

echmea as well as for most genera of the subfamily
Eu 1934). The taxonomic boundaries that sep-

arate Aechmea from other Bromelioideae genera are
vague and in need of revision. This was noted by
early taxonomists (Baker, 1879, 1889; Mez, 1892,
1896, 1935) and remains true in the last revision
(Smith & Downs, 1979), where some species of
Ronnbergia E. Morren & André, Quesnelia Gau-
dich., and Streptocalyx Beer appear within identi-
fication keys for Aechmea. According to the con-
ceptual limit of Aechmea (sensu Smith & Downs,
1979) species placement often seems arbitrary with
several species from other genera easily placed
within Aechmea and vice versa. Such examples in-
clude the transfer of all Streptocalyx species into
Aechmea (Smith & Spencer, 1992), as well as the
transfer of species traditionally treated in Aechmea
to other genera, e.g., Lymania Read (1984) and Ur-
sulaea Read & Baensch (1994). Smith and Downs
(1979) divided Aechmea into eight subgenera: Aech-
mea, Podaechmea Mez, Platyaechmea (Baker) Bak-

The n thank the following for p in apii iu. anm material: C. M. Vieira,

. C. Gurken (in me ерюн), НА

M. de Mello, Н. Luther, 5. Potsch, and А a. Thanks . Barth for ape di + aa facilities and help in
b верн to 1. Brown for 5 and Dies support during Faria's and Wendt’s visits ч Laramie,
Wyoming; reviewers E. J. m and G. Zizka, and editor V. C. Hollowell for constructive comments. This paper

represents a portion of the M.S
CAPES, Pronex-Finep,

? Departamento de jm
Janeiro-RJ, Brazil. twendtGbiclogia. ufrj

. dissertation of the first author. We gratefully acknowledge various support from CNPq,
bd Bromeliad Society International, and the National Science Foundation (DEB-0129446).
oe Federal do Rio de Janeiro, IB, CCS, Ilha do Fundão, 21941-590, Rio de

Department of Botany, University of Wyoming, Laramie, Wyoming 82071, U.S.A., and Marie Selby Botanical Garden,

Sarasota, Florida 34236-7726, U.S.A.

ANN. Missouni Bor. GARD. 91:

303—319. 2004.

Annals of the
Missouri Botanical Garden

r, Ortgiesia (Regel) Mez, Pothuava (Baker) Baker,
iai occus (Beer) Baker, Macrochordion (de

riese) Baker, and Chevaliera (Gaudich. ex Beer)
Baker, and later Smith and Kress (1989, 1990) el-
evated or resurrected all of them to generic level.
However, the taxonomic changes proposed by
Smith and Kress (1989, 1990) were not followed by
other authors (Luther & Sieff, 1994; Wendt, 1997;
Luther, 2000)

In Aechmea two reasons emerge for discordant
classifications. First, monographers have stressed
only a few characters, and those characters differ
from author to author. Second, this problem is am-
plified by the limited knowledge of many poten-
tially useful diagnostic characters. For example, the
intracalyx floral morphology is either poorly pre-
served or not preserved at all in herbarium collec-
tions and therefore remains scantily understood.
Consequently, past monographs relied heavily on
vegetative, inflorescence, sepal, and floral bract
features that are observed on herbarium specimens.
The importance of fresh or liquid-preserved mate-
rial for morphological analysis of reproductive
structures has been stressed (Utley, 1983; Brown &
Gilmartin, 1984; Leme, 2000

Recent advances in the systematics of Bromeli-
aceae have been realized using cladistic analyses
of molecular and morphological data. These works
have addressed phylogenetic relationships between
the subfamilies (Ranker et al., 1990; Terry et al.,

; Horres et al., 2000) and genera of Tilland-
sioideae (Gilmartin & Brown, 1986; Terry & Brown,
1997) and Pitcairnioideae (Varadarajan & Gilmar-
tin, 1988). The monophyly of Bromelioideae is well
supported by cladistic analysis based on morpho-
logical and molecular data (Ranker et al., 1990;
1997; Horres et al., 2000). However,
at a generic level, except for work by Ramírez

Terry et al.,

(1996) that used morphological characters to ex-
plore the sister taxon relationships and the putative
monophyletic status for Cryptanthus Otto €
iet, and by Brown and Leme (2000) that pre-
sented a cladistic analysis of Nidularium Lem. and
related Bromelioideae genera (Wittrockia Lindm.,
Neoregelia L. B. Sm.,
istropsis Mez (ете), Edmundoa Leme), there is no

Canistrum E. Morren, Can-
known cladistic study within Bromelioideae involv-
ing the taxa analyzed in this work (i.e., Aechmea
and related genera).

The main objectives of this paper were to inves-
tigate the phylogenetic position of Aechmea and
other related genera of Bromelioideae, and to assess
the validity of past infrageneric classifications pro-
posed for Aechmea (Baker, 1889; Mez, 1892, 1890,
1935; Smith & Downs, 1979; Smith & Kress, 1989,

1990; Smith & Spencer, 1992). We also hope to
improve knowledge of Bromelioideae morphology
by including underutilized and new character data.

MATERIALS AND METHODS
TAXON SAMPLING

A total of 86 taxa (83 species and 3 varieties)
representing 7 of the 8 subgenera of Aechmea (50
spp., 2 var.), as well as the genera Acanthostachys
Klotzsch (2 spp.), Billbergia Thunb. (6 spp.), Fern-
seea Baker (1 sp.), Lymania (1 sp.), Hohenbergia
Schult. f. (5 spp.), Portea Brongn. ex Koch (4 spp.).
Quesnelia (9 spp., 1 var.), Ronnbergia (2 spp.), and
Streptocalyx (3 spp.), were sampled as ingroups (Ta-
ble 1). These latter genera were selected because
they have a clear morphological affinity to Aechmea
and are themselves weakly delimited. Species were
sampled to include as much as possible the known
morphological and geographic variation of each ge-

-

ius or subgenus analyzed. Specimens were col-
lected in the field or obtained from living collec-
tions in Brazil. For those cultivated samples listed
in Table 1, horticultural cultivars and hybrids were
avoided, using only specimens previously collected
from the wild. Exemplar specimens (one or two
specimens per species or variety) were used for the
scoring of character states. In. 7596 of the genera
and subgenera sampled it was possible to include
the type species. Voucher specimens are listed in
Table 1, and a summary of the representative per-
centage for each taxon sampled is presented in Ta-
ble 2.

Two species from the genus Cryptanthus were se-
lected as the cd on the basis of recent mo-
T , 1997) that placed Cryp-
tanthus in a basal dd relative to those ingroup

lecular work (Terry
genera analyzed here.

MORPHOLOGICAL DATA

A total of 60 characters were coded, including
13 vegetative, 46 reproductive, and 1 pollen char-
The characters and their states used in this
79 taxa

acter.
analysis are presented in Appendix 1. For 7
(including the outgroup), all floral characters and
some leaf characters such as ornamentation and
number were scored from living plants or flowers
preserved in 70% alcohol. The remaining charac-
ters were determined after preparing the herbarium
voucher. For 7 species (Aechmea allenii, A. drak-
eana, A. fraseri, A. involucrata, А. mariae-reginae,
Ronnbergia deleonii, and К. morreniana), all mor-
phological data were obtained from herbarium
specimens (SEL), complemented with photos of liv-

Volume 91, Number 2 Faria eta
2004

Cladistic Relationships of Aechmea

Table 1. Taxa used in the phylogenetic analysis. Type species of genera and subgenera are indicated in bold.
Smith and Downs

Subgeneric ass ts correspond to the traditional classification of Bromelioideae, sensu

ignm ‹
(1979). Voucher 5 includes collector with number, and herbarium code. * Indicates plants collected

from cultivation.

Taxon Geographic origin

Voucher

Acanthostachys Klotzsch

A. pitcairnioides (Mez) Rauh & Barthlott Brazil, Bahia*
A strobilacea (Schult. f.) Klotzsch Eastern Brazil*
Brazil, Parana
Aechmea subg. Aechmea Ruiz & Pav.
A. angustifolia Poepp. & Endl. Costa Rica*
A. aquilega (Salisb.) Griseb. Brazil, Paraíba*
blanchetiana (Baker) L. B. Sm. Brazil, Bahia*
A. correia-araujoi E. Pereira & Moutinho Brazil, Bahia*
A. eurycorymbus Harms Brazil, Pernambuco*
Brazil, Pernambuco*
A. fosteriana L. B. Sm. Brazil, Espirito Santo*
Brazil, Espírito Santo*
A. gurkeniana E. Pereira & Moutinho Brazil, Bahia*
Brazil. Bahia*
A. lingulata (L.) Baker Brazil, Rio de Janeiro
A. marauensis Leme Brazil, Bahia*
A. mutica L. B. Sm. Brazil, Espirito Santo*
Brazil, Espirito Santo
А. orlandiana L. В. Sm. Brazil, Espirito Santo*
Brazil, Espirito Santo*
A. penduliflora André Costa Rica*
A. purpureorosea (Hook.) Wawra Brazil, Rio de Janeiro*
A. ramosa var. festiva L. B. Sm. Brazil, Espirito Santo*
Brazil, Espirito Santo*
A. ramosa var. ramosa Mart. ex Schult. f. Brazil, Espirito Santo
A. rubens ~ B. Sm.) L. B. Sm. Northeast Brazil*
A. stelligera L. B. Sm. Northeast Brazil*
A. w 5 Harms Brazil, Pernambuco*

Aechmea subg. Chevaliera (Gaudich. ex Beer) Baker

A. multiflora L. В. Sm. Brazil*
A. saxicola L. B. Sm. Brazil, Espirito Santo
A. sphaerocephala Baker razil, Rio de Janeiro

Aechmea subg. Lamprococcus (Beer) Baker

A. fulgens Brongn. Brazil, Bahia*
A. miniata жае hort. ex Baker Brazil, Bahia*
A. warasii E. Pereira Brazil, Espirito Santo*
A. weilbachii var. c mI Leme & A. Costa Brazil, Rio de Janeiro*
A. weilbachii var. weilbachii Didrichsen Brazil, Rio de Janeiro*

Aechmea subg. Macrochordion (de Vriese) Baker
. bromeliifolia sed Baker Brazil, Espirito Santo*
A. triangularis L. Brazil, Espirito Santo

Aechmea subg. Ortgiesia (Regel) Mez

A. burle-marxii E. Pereira Brazil, Bahia*

A. calyculata (E. Morren) Baker Brazil, Santa Catarina*
A. coelestis (K. Koch) E. Morren Brazil, Espírito Santo
A. gamosepala Wittm. Southern Brazil*

A. recurvata (Klotzsch) L. B. Sm. Southern Brazil*

Southern Brazil*

Faria 03 (REA)
Faria 02

Hatschbach 12933 (RFA)

Wendt 346 (RFA)
Vieira 1249 (RFA)
Faria 13 (RFA)
Vieira 1247 (RFA)
Vieira 1250 (RFA)
Faria 14 (RFA)
Vieira 1217 (RFA)
Faria 34 (RFA)
Vieira 1212 (RFA)
Faria 33 (RFA)
Faria 30 (RFA)
Faria 18 (RFA)
Wendt 375 (RFA)
Faria 26 (RFA)
Vieira 1219 (RFA)
Faria 32 (RFA)
Vieira 1275 (RFA)
Vieira 1256 (RFA)
Vieira ip (RFA)

Faria 17
Faria 16

Canela 02 (RFA)
Faria 27 (RFA)
Wendt 330 (RFA)

Vieira 1252 (RFA)
Vieira 1259 (RFA)
Vieira 1267 (RFA)
Costa s.n. )

Vieira 1208 (RFA)

Faria 39 (RFA)
Wendt 392 (RFA)

Wendt p оч
Vieira 1221 (RFA)
Vies A 16 (RFA)

Wendt 351 (RFA)
Faria 31 (RFA)
Faria 45 (RFA)

Annals of the

Missouri Botanical Garden

Table 1. Continued.

Taxon

Geographic origin

Voucher

Aechmea subg. Platyaechmea (Baker) Baker
A. caesia E. Morren ex Baker
A. chantinii (Carriére) Baker
A. dealbata E. Morren ex Baker
А. 3 Lem
A. fasciata (Lindl.) Baker
Aechmea subg. Pothuava (Baker) Baker
A. allenii L. B. Sm.
A. alopecurus Mez
A. bocainensis E. Pereira & Leme
A. brueggeri Lem
A. drakeana An "
A. fraseri Baker

A. guarapariensis E. Pereira & Leme
A. involucrata André

. mariae-reginae H. Wendl.
ў nudicaulis T ) Griseb.
A. ornata Bake

A. pectinata Baker
A. pineliana (Brongn. ex Planch.) Baker

A. vanhoutteana (Nan Houtte) Mez

Billbergia subg. Billbergia Thunb.
B. amoena (Lodd.) Lindl.
B. distachia (Vell.) Mez
B. elegans jane ex 5 f.
. euphemia
B. раан еа ai

B. sanderiana E. Morren
Cryptanthus Otto & A. Dietr.

C. bromelioides o & A. Dietr.

C. pickelii L. B.
Fernseea Baker

F. itatiaiae (Wawra) Baker
Hohenbergia subg. Hohenbergia Schult. f.
catingae Ule
. correia-araujoi E. Pereira & Moutinho

mm

disjuncta L. B. Sm.
ramageana Mez

. stellata Schult.f.

* * *

Lymania Read
L. azurea Leme

Portea Brongn. ex K. Koch
P. alatisepala Philcox
P. fosteriana L. B. Sm

Brazil, Rio de Janeiro*
Brazil, igni nas*
Brazil, Rio de Janeiro*
Brazil, Sao Paulo*
Brazil, Rio de Janeiro*

и

Brazil,

Brazil, MS
Brazil, Minas Gerais*

Ecuador

Brazil, Rio de Janeiro
razil, Paraná
Brazil, Rio de Janeiro
Brazil, Rio de Janeiro
Brazil, Espirito Santo*
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro
Brazil, Rio de Janeiro

Eastern Brazil*
Southern 71

Brazil, Espírito Santo*
Brazil, Espírito Santo
Brazil, Rio de Janeiro
Brazil, Rio de Janeiro
Brazil, Espírito Santo

Brazil, Rio de Janeiro
Brazil, Pernambuco*

Brazil, Rio de Janeiro

Brazil, Bahia*

a
Brazil, Bahia*
Brazil, Bahia*

Brazil, Bahia
Brazil, inl Santo

Vieira 1211 (RFA)

Faria 10 (RFA)
Vieira 1246 (RFA)

Luther s.n. (SEL)

Girko E90-195J (SEL)
Kessler 2414 (SEL)
Luther s.n. (SEL)
Wendt 349 (RFA)
Berg s.n. (SEL)
Cathcart s.n. (SEL)
Meerow s.n. (SE zd
Sampaio s.n. (RFA
Wendt 290 (R P
Wendt 365 (RFA)
Wendt 334 (RFA)
Vieira 1213 (RFA)
Faria 40 (RFA)
Ribeiro s.n. (RFA)
Wendt 372 (RFA)

Faria 08 (RFA)

Wendt 388 (RFA)
Wendt 360 (RFA)
Faria 28 (RFA)

Wendt 389 (RFA)

Rocas s.n. (RFA)
Faria 38 (RFA)

Ribeiro 291 (RFA)

Wendt 352 (RFA)
Vieira 1254 (RFA)
Wendt 344 (RFA)
Wendt 336 (RFA)
Pereira 9625 (RFA)
Vieira 1270 (RFA)

Faria 44 (RFA)

Faria 20 (RFA)
Wendt 396 (RFA)

Volume 91, Number 2

Faria et al.
Cladistic Relationships of Aechmea

307

Table 1. Continued.

Taxon

Geographic origin

Voucher

P. leptantha Harms

P. petropolitana (Wawra) Mez
Quesnelia subg. Billbergiopsis Mez

Q. augusto-coburgii Wawra

Q. blanda Mez

Q. edmundoi var. edmundoi L. B. Sm.

Q. edmundoi var. rubrobracteata E. Pereira

Q. lateralis W

Q. liboniana (De Jonghe) Mez

O. marmorata (Lem.) Rea

O. seideliana L. B. Sm. & Reitz
Quesnelia subg. Quesnelia Gaudich.

Q. arvensis (Vell.) Mez

O. quesneliana (Brongn.) L. B. Sm.

Ronnbergia E. Morren & André
К. deleonii L. B. Sm
R. morreniana L айви & André
Streptocalyx Beer
S. floribundus (Mart. ex Schult. f.) Mez
S. longifolius (Rudge) Baker
S. poeppigii Beer

Brazil, Espírito Santo
Brazil, Bahia*

Brazil, Bahia*

Brazil, Rio de Janeiro*

Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro

Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*

Brazil, Rio de Janeiro
Brazil, Rio de Janeiro*
Brazil, Rio de Janeiro*

Ecuador
Ecuador

Brazil, Rio de Janeiro
Brazil, Amazonas*
Brazil, Amazonas*
Brazil, reia

Wendt 397 (RFA)
Vieira 1248 (RFA)
Faria 15 (RFA)
Faria 09 (RFA)

Vieira 98S (RB)
Vieira s.n. (RB)
Vieira 873A (RB)
Gurken 1552 (RB)
Vieira 1206 (RB)
Vieira 1210 (RB)
Faria 01 (RFA)
Vieira 968 (RB)

Vieira 1234 (RB)
Gurken 1546 (RB)
Gurken 1543 (RB)

Luther s.n. (SEL)

Determann s.n. (SEL)

Faria 29 (RFA)
Vieira 1269 (RFA)
Vieira 1255 (RFA)
Wendt 350 (RFA)

ing material. The pollen data were taken from the
available literature (Ehler & Schill, 1973; Erdtman
& Praglowski, 1974; Wanderley & Melhem, 1991;
Halbritter, 1992; Sousa et al., 1997) and scored
from herbarium or liquid-preserved samples using
the methods described by Wodehouse (1935). Con-
tinuous variables (e.g.. mature leaf length) were as-
sessed as discrete variables based on observed dis-
continuous gaps between species.

PHYLOGENETIC ANALYSES

Data were entered into a matrix using the com-
uter program MacClade 4.0 (Maddison & Maddi-
son, 2000), and the phylogenetic analyses were per-
formed with PAUP* 4.0b10 (Swofford, 2001). In the
data matrix (Appendix 2), missing character states
(0.2%) are indicated with a question mark, and in-
applicable character states (3.4%) are indicated
with a dash. The large size of this data matrix man-
dated use of a heuristic search strategy designed to
discover islands of most parsimonious trees. These
rches were conducted following Olmstead et al.
(1993) and Olmstead and Palmer (1994). All char-

acters were unweighted, and multistate characters

were treated as unordered. To evaluate the support
for each node, 100 bootstrap replicates with ful
heuristic search were conducted. Relative levels of
homoplasy and synapomorphy in the data sets were
calculated using the consistency index (CI), the re-
tention index (RI), and the rescaled consistency in-
dex (RC) as implemented in PAUP* 4.0b10. Char-
acter state. changes were mapped on the strict
consensus tree using MacClade (Maddison & Mad-
dison, 2000
RESULTS

The cladistic analysis yielded 158 equally most
parsimonious trees of 777 steps length, with 59 in-
of
0.142 excluding autapomorphies, a retention index
(RI) of 0.606,
(RC) of 0.086.
in Figure 1. The ingroup is well supported as mono-

—

formative characters, a consistency index (СГ

and a rescaled consistency index
The strict consensus tree is shown
phyletic within a bootstrap value of 100% (Fig. 1),
but most internal support was less than 50%.
This analysis supports the monophyly of four
Billbergia, Portea, and

genera: Acanthostachys,

Ronnbergia and two subgenera of Aechmea: Chev-

308 Annals of the
Missouri Botanical Garden
Table 2. Percentage of genera and subgenera sampled for ingroups in this study.
No. of No. of taxa Percentage
Genus/Subgenus* species^ sampled sampled*
Genus e Klotzsch 2 2 100%
Genus Aechmea Ruiz & Pav 222 52 23%
Subgenus Aec dne Ruiz & P 107 18 17%
Subgenus Chevaliera (Gaudich. « ex о Вакег 23 3 13%
ici Lamprococcus (Beer) B 16 > 31%
ubgenus Macrochordion (de ане Вакег 11 2 18%
Subgenus Ortgiesia (Regel) Mez 21 5 24%
Subgenus Platyaechmea (Baker) Baker 18 5 28%
Subgenus Pothuava (Baker) Baker 21 14 67%
Subgenus Podaechmea Mez 5 0 МА
Genus Bill ia T b. 62 6 10%
Subgenus Billbergia Thunb. 37 6 16%
Subgenus Helicodea Aaji ) Baker 25 0 NA
Genus Fernse 2 1 50%
Genus Hohe ibn Se an It. f. 50 10%
Subgenus Hohenbergia Schult. f. 30 5 17%
Subgenus Wittmac kiopsis Mez 20 0 NA
Genus Lymania Read 7 1 14%
Genus Portea Brongn. ex K. Koch 9 4 44%
Genus Quesnelia Gaudic 15 10 56%
Subgenus Quesnelia Gaudich. 2 2 100%
Subgenus patel ea Mez 13 8 62%
Genus Ron a E. Morren & André 11 2 18%
Genus poda Beer 15 3 20%

a Classification follows Smith and Downs (1979) except for Lymania (Read, 1984) and Acanthostachys (Rauh
2)

& Barthlott, 198
"Luther and Sieff
NA = not applicab

1997); Luther (2001).

aliera and Macrochordion (Fig. 1). Based on our
sample, Hohenbergia appears paraphyletic, Lyman-
ia is placed within Aechmea, and Fernseea is the
sister taxon to Billbergia (Fig. 1). Streptocalyx,
Quesnelia, and the remaining subgenera of Aech-
mea are polyphyletic (Fig. 1). Most characters an-
alyzed displayed high levels of homoplasy (Table
3). These results support particular elements of
but do not agree
1). In the con-

some previous classifications,
closely with any one treatment (Fig.

sensus tree, nine clades have been identified (Fig.

DISCUSSION

The only generic-level, morphologically based

cladistic studies in subfamily Bromelioideae
(Brown & Leme, 2000; this study) display two com-
mon features. First, consensus trees have notably
more resolved nodes than unresolved ones. Second,
bootstrap support is lacking (i.e., < 50%) for most
of the resolved clades. We have somewhat arbitrari-
ly recognized nine clades that will focus the follow-

ing discussion.

CLADE |

Our results suggest that the genus Acanthostach-
ys (Fig. Smith and Downs
(1979) recognized only one species for the genus.
The second, A. pitcairnioides, was previously treat-
ed within Aechmea subgenera Ortgiesia (Mez, 1896)
or Pothuava (Smith & Downs, 1979) and later
transferred to Acanthostachys by Rauh and Barth-
lott (1982), and our analyses support this treatment.
Acanthostachys strobilacea and A, pitcairnioides dif-
fer greatly in flower and inflorescence morphology.
Most of the synapomorphies that define the Acan-
thostachys clade are vegetative features (characters
6, filiform leaf blades; 9, long-attenuate leaf apex;
13, scape bracts not imbricate; 34, terminal spine
shorter than the floral bract length; 37, concave flo-
ral bracts; 60, rosette not forming a water impound-

1) is monophyletic.

ing tank). Filiform leaf blades is the only apo-
morphic character unique for this genus, but this
leaf morphology can also be found in species of
other bromelioid genera (Orthophytum Beer, Bro-
melia L., Ananas Mill.), which were not included
in this study. Tomlinson (1969) suggested that this

Volume 91, Number 2
004

Faria et al.
Cladistic Relationsh

309
ips of Aechmea

A. pitcairnioides ~~
J | CLADE 1 ll Acanthostachys
A. angustifolia — ^ 77V
A. pedea deas Aechmea sg. Aechmea
H. disjuncta
H. correia-araujoi |
Н. catingae Hohenbergia
H. stellata
H. ramageana
A. stelligera
A. aquileg.
A. rubens A. sg. Aechmea
E A. blanchetiana
A. corymbus
P. alatsepala
P. fosteria
Р. petropolitana Portea
P. leptant
A. werdermannii
ramosa ra
osa var. festiva A. sg. Aechmea
A. purpureorosea
rcs longifoliu Streptocalyx
S. poeppigii
EU. jo la i: albipetala CLADE 2 A. sg. HANS
A. pendu A. sg. Aec
A. perit A. sg. 7
A. caesia
A. dealbata A. sg. Platyaechmea
A. fasciata
Q. marmorata Quesnelia
7 A. fulgens
4 A. warasii A. sg. Lamprococcus
A. Бы
L.a Lymania
f à correla-ar araujoi A. sg. Aechmea
A. chantinii A. sg. Platyaechmea
Q. edmundo var. rubrobracteata Quesnelia
A. fost
= — ‚ gurkeniana A. ag. Aechmea
weilbachii var. weilbachii A. sg. Lamprococcus
A ntha A 5 „
тиса. a ل‎
ШШ ptc E vanhouttea А т P au || РМ sg. Pothuava
Q. edmundoi var. edmundoi
04 ‹ . arvensis CLADE 3 Quesnelia
Q. quesneliana = ____-----------------4
borane A. sg. Pothuava
A. calyculata |— "^ —
rC A. gamosepala Jeraoe 4 A. sg. Ortgiesia
| Ш А. recurvat
llenii
drakeana A. sg. Pothuava
sanderiana
amoena
ans " Ў
Я distachia Billbergia
. euphemiae
— E pyramidalis CLADE 5 -
ernse
burgii Quesnella
A. fi e
A. involucrata A. sg. Pothuava
Q. liboniana
Q. lateralis ;
| sei Allana Quesnelia
. Blanda ———— tme
nudicaulis A. sg. Pothuava
A. saxicola
ШИЛ ши тиш [cae 6 A. sg. Chevaliera
1 A
A. bromeliifolia
— 4 triangularis — J clave 7 A. sg. Macrochordion
pecurus
guarapariensis
r
marias reginae A. sg. Pothuava
pectinata
pineliana
brueggeri
59 R. deleonii — ^ А
Er morreniana NETUS. | l CLADE 8 Ronnbergia
A. lingulata = == A. sg. Aechmea
| _ +; . burle-marxii [crane 9 A. sg. Ortgiesia
o: 3 W — — — Streptocalyx
g= С. pickelli
C Added | ШП | OUTGROUPS f Cryptanthus

Figure J.

produced by cladistic analysis of morphological charac
are discussed in the text. Numbers above branches are the bootstra

Strict consensus of 158 equally most parsimonious trees of

=>”

ER.

ap percentages (of over 50%).

steps for Aechmea and related genera
ters. Genus Cryptanthus was us ee as outgroup. Clades 1 to €

T he most recent gene ric

and infrageneric delimitation proposed for eo. Bromelioideae (Smith & Downs, 1925 Rauh & Barthlott, 1982;
Read, 1984) is shown beside the black ba

310 Annals of the
Missouri Botanical Garden

e 3. Number of states, number of steps, and consistency (CI), retention (RI), and rescaled consistency
e es of 60 morphological characters estimated by character diagnostic analysis. Characters are listed
according to descending RC values; character numbers refer to those presented in Appendices | and 2.

Character States Steps CI RI RC
6. Leaf form 3 2 1.00 1.00 1.00
29. Floral bract presence 2 1 1 1.00 1.00
56. Filament shape 2 2 0.50 0.86 0.43
54. Ovary surface 3 4 0.50 0.80 0.40
39. Pedicel 2 2 0.50 0.75 0.38
28. Primary bract apex 3 5 0.40 0.93 0.37
24. Primary bract presence 2 3 0.3 0.94 0.32
10. A false midrib 2 2 0.50 0.50 0.25
26. Primary bract color 3 8 0.25 0.87 0.22
27. Primary bract texture 2 8 0.25 0.87 0.22
21. Inflorescence type 4 12 0.25 0.83 0.21
52. Petal orientation at anthesis 3 7 0.29 0.72 0.21
58. Types of pollen grains 6 19 0.21 0.58 0.12
25. mary bract margi 2 13 0.15 0.78 0.12
31. Floral bract color 4 20 0.20 0.56 0.11
36. Floral bract carinate 3 13 0.23 0.47 0.11
34. Terminal s guak in = apex of the floral bract 3 17 0.18 0.59 0.10
30. Floral bract ma 2 9 0.22 0.46 0.10
14. Scape ане differentiation into sheaths and blades 2 4 0.25 0.40 0.10
41. Sepal co 5 26 0.15 0.56 0.09
55. Ovary pl 4 15 0.20 0.43 0.09
. Leaf margin 2 6 0.17 0.50 0.08
43. Terminal spine apex of the sepals 3 16 0.13 0.64 0.08
1. Mature leaf length 3 17 0.12 0.62 0.07
35. Floral bract shape (length/width ratio) 4 29 0.14 0.50 0.07
22. Flowers congested on rachis or inflorescence branches 2 11 0.09 0.75 0.07
32. Floral bract texture 2 15 0.13 0.50 0.07
37. Shape of floral bract relative to the flower 2 18 0.11 0.60 0.07
60. Rosette forming a water impounding tank 2 5 0.20 0.33 0.07
50. Petal appendage 4 25 0.12 0.53 0.06
47. Petal color 5 28 0.14 0.44 0.06
40. Flower indumentu 3 17 0.12 0.53 0.06
53. Ovary cross eon 3 20 0.10 0.61 0.06
33. Floral bract apex (excluding terminal spine) 3 27 0.11 0.53 0.06
12. Scape 3 10 0.20 0.27 0.06
18. Scape ien apex (excluding the terminal spine) 3 8 0.13 0.42 0.05
48. Petal a 3 22 0.09 0.57 0.05
20. Ca cate rachis color 2 14 0.07 0.67 0.05
23. нй arrangement along the rachis or inflorescence
branches 2 10 0.10 0.47 0.05
51. Petal with lateral folds on the adaxial surface 2 13 0.08 0.59 0.05
3. Number of leaves per rosette 3 22 0 0.47 0.04
19. Inflorescence length excluding the naked scape (cm) 3 25 0.08 0.53 0.04
17. Scape bract texture 2 11 0.09 0.44 0.04
59. Habit 2 5 0.20 0.20 0.04
9. Leaf apex P (excluding terminal spine) 4 19 0.16 0.24 0.04
15. Scape E 2 15 0.07 0.58 0.04
13. Scape b 2 16 0.06 0.56 0.04
38. Flower length (without the pedicels) 3 28 0.07 0.49 0.04
45. Sepals ca 2 12 0.08 0.39 0.03
4. Leaf ornamen n tio 2 0.11 0.27 0.03
57. Filament adnation m petals 3 28 0.07 0.40 0.03
16. Scape bract color 2 18 0 0.49 0.03
49. Petal sha 2 20 0.05 0.55 0.03
44. Sepal sym 2 19 0.05 0.47 0.03
8. siena E lacs per 5 cm length of margin 3 27 0.07 0.29 0.02
42. Sepal a 2 21 0.05 0.44 0.02
2. Blade m sheath 2 14 0.07 0.28 0.02
46. Sepal connation 2 13 0.08 0.25 0.02
5. Alteration in leaf color during anthesis 2 2 0.50 0 0
11. Phyllotaxy 2 1 1.00 0 0

Volume 91, Number 2

Faria et al.
Cladistic Relationships of Aechmea

is a xeromorphic character, and as such, possesses
more ecological than taxonomic significance.

CLADE 2

This is a large and highly heterogeneous clade
(Fig. 1) containing members of four Aechmea sub-
Pla-
tyaechmea) and four additional genera (Hohenber-
gia, Portea, Streptocalyx, Quesnelia). The genera
Hohenbergia and Portea as well as Aechmea subg.

genera (Aechmea, Lamprococcus, Ortgiesia,

Lamprococcus and Platyaechmea are restricted to
this clade. All other included genera and subgenera
have representatives in other clades as well.

All investigated species of Hohenbergia (5 of 50
spp. sampled) are found in an unsupported group
that also includes three species of Aechmea subg.
Aechmea. Aechmea marauensis is placed as sister
species of H. disjuncta, while two other species
within subgenus Aechmea (A. angustifolia and A.
stelligera) have a more basal position in this sub-
clade. Traditionally, Hohenbergia is characterized
by its inflorescence pattern with multiple branches,
congested flowers, and floral bracts covering ovaries
and sepals (Smith & Downs, 1979). Of these char-
acters, the synapomorphies of twice (or more)
branching inflorescences and congested flowers
(characters 21 and 22,
clade formed by Hohenbergia species plus A. mar-

respectively) define the

auensis. Hohenbergia has been treated as closely
related to Aechmea subg. Aechmea, or placed as a
separate subgenus or section of Aechmea (Baker,
1879, 1889). Our analysis has some agreement with
the old classifications proposed by Baker (1879,
1889); however, additional sampling within Hoh-
enbergia is needed.

The genus Portea (4 of 9 species sampled) also
forms an unsupported clade nested within Aechmea,
clade 2 (Fig. 1). Portea, like Hohenbergia subg.
Hohenbergia, is restricted in distribution to the east
coast of Brazil (northeast and southeast regions),
and it shares many morphological characters with
species of Aechmea subg. Aechmea. Ported petro-
politana was treated within subgenus Aechmea by
Baker (1889). Due to its multiporate pollen, Mez
(1892, 1896, 1935) considered Portea to be closely
related to Gravisia,
Aechmea (Smith & Downs, 1979).

Two of three Streptocalyx species (3 of 14 total)
in our analysis also occur in an unsupported clade
nested within Aechmea. The third species (S. flo-
ribundus) is found in clade 9 (Fig. 1), the basal-
most clade in the ingroup. Streptoc alyx has been
treated as a distinct genus (e.g., Smith & Downs,
1979) or submerged within Aechmea (Smith &

a genus synonymized under

Spencer, 1992). Our results suggest that Strepto-
calyx (sensu Smith & Downs, 1979) may not be
monophyletic, and that this taxon has affinities with
at least two distinctly different elements of Aech-
теа.

Only one species of Lymania (7 total) was in-
cluded here. Lymania is generally accepted
monophyletic based on а sulcate ovary (Read,
1984), and a syndrome of floral and vegetative
characters. Species of Lymania have either been
recently described in the genus or transferred from
either Aechmea subg. Lamprococcus or from the ge-
nus Araeococcus Brongn. The only exemplar in-
cluded here is in the most strongly supported clade
(94% bootstrap) within the ingroup, along with
three species of subgenus Lamprococcus.

CLADE 3

This clade (Fig. 1) consists of Quesnelia arvensis
and Q. quesneliana (subg. Quesnelia) on a well sup-
ported branch (bootstrap of 91%) with Aechmea
vanhoutteana (subg. Pothuava) and Q. edmundoi
var. edumundoi (subg. Billbergiopsis) as the sister
group.
quesneliana, and A. vanhoutteana was already not-
ed by Baker (1879, 1889), who treated A. van-
Wendt (1997) also
stressed the close relationship among these species,

The close affinity among Q. arvensis, Q.

houtteana within Quesnelia.

based on the pattern of inflorescence and charac-
ters related to scape, floral bracts, petals, and petal
appendages. Clade 3 is defined by a single homo-
plasious synapomorphy (character 16, pale or green
scape bracts) and received no significant bootstrap
support.

CLADE 4

Formed by three species of Aechmea subg. Ort-
giesia (Fig. 1), this clade is supported by two hom-
oplasious synapomorphies (characters 44, ше t-
ric or slightly asymmetric onnate
sepals above 1/3 of their length). ais connate
sepals has been a diagnostic character for Aechmea
subg. Ortgiesia by Mez (1892, 1896, 1935) and
Smith and Downs (1979), the monophyly of the en-
tire subgenus is not supported by our results. Two
other Ortgiesia members (А. burle-marxii, A. coe-
lestis) were placed distantly from each other as well
as clade 4.

CLADE 5

This clade (Fig. 1) comprises species of Aechmea
(subg. Pothuava), Billbergia, Fernseea, and Ques-

E

nelia (subg. Billbergiopsis). Clade 5 is defined by

Annals of the
Missouri Botanical Garden

two homoplasious synapomorphies (characters 38,
flowers longer than 3.5 cm; 42, acute sepals). The
genus Billbergia (6 of 62 sampled) appears mono-
phyletic with a close relationship to Fernseea. The
synapomorphies supporting Billbergia are all floral
(characters 33, rounded floral bract apex; 35,
broadly ovate floral bracts; 42, rounded sepal apex:
52, recurved petals in anthesis; 55, white or green
ovaries; 56, filiform filaments), though only re-
curved petals have been previously used as a di-
agnostic character for the genus (Smith & Downs,
1979). The close relationship between Billbergia
and Fernseea is supported by the presence of col-
pate pollen grains (character 58), among other syn-
apomorphies (characters 16, rose or red scape
bracts; 43, terminal spine of the sepals absent or
much reduced; 44, sepals symmetric or slightly
asymmetric; 47, red or rose petals; 48, rounded pet-
al apex).
1896, 1935), who placed these two genera in sub-

This is in agreement with Mez (1892,

tribe Sulcatae due to this particular pollen mor-
phology.

Species from Aechmea subg. Pothuava and Ques-
nelia subg. Billbergiopis comprise the remainder of
clade 5. The polyphyletic status for both Aechmea
subg. Pothuava and Quesnelia (Fig. 1) is reflected
both by disjunct positions of member taxa on the
consensus tree, and by the number of additional
steps to make these taxa monophyletic (76 steps for
Pothuava; 35 steps for Quesnelia). Aechmea subg.
Pothuava has been variably treated at the generic,
sectional, and subgeneric levels within Aechmea
1997)

consists of ca. 20 species occurring in two centers

(see review in Wendt, . Subgenus Pothuava
of geographic distribution: one in southern Brazil
and the other in northwestern South America into
Central America (Smith & Downs, 1979). Species
distributed in these two centers possess very few
morphological affinities but have been 5
97). The

placement of subgenus Pothuava species on the

treated in the same subgenus (Wendt,

consensus tree may correlate with the disjunct pat-
tern of distribution observed for the subgenus.
Those species of subgenus Pothuava in clade 5 (A.
allenii, A. drakeana, A. fraseri, A. involucrata) are
from western South America and Central America,
whereas the Brazilian Pothuava species (A. alope-
curus, A. bocainensis, A. brueggeri, А. guaraparien-
sis, A. ornata, A, pineltana, A. pectinata, A.

—

an-
houtteana) show unresolved relationship or lie in
other clades.

Baker (1889) and Mez (1892, 1896) were the
first authors to argue that Quesnelia constitutes a
natural group. Mez (1892, 1896) stressed that Ques-
nelia subg. Billbergiopsis shows greater affinity to

Billbergia than to Quesnelia subg. Quesnelia. Our
results suggest that Quesnelia (sensu Smith &
Downs, 1979

—

may not be monophyletic.

CLADE 6

The three sampled species of subgenus Cheva-
liera are placed in a moderately supported clade
(bs. 76%; Fig. 1). Chevaliera sensu Smith and
Downs (1979) is characterized by the lack of, or
reduction in, petal appendages. From the synapo-
morphies that define clade 6 (characters 1, leaves
greater than 100 cm; 7, leaf margin with spines
greater than 3 mm; 34, terminal spines not exceed-
ing floral bract length; 45, sepals with keels; 57,
filaments adnate to the petals from their mid-point),
none had previously been used as diagnostic. Re-
lationship between Chevaliera and the other clades
is unresolved in the consensus tree.

CLADE 7

Only 2 of 11 species of Aechmea subg. Macro-
chordion were sampled, but the results suggest that
this subgenus may be monophyletic (Fig. 1). Syn-
apomorphies that define the group include these
characters (32, coriaceous floral bract; 40, dense
indumentum covering floral parts; 43, unarmed se-
pals; 53, circular ovaries). Smith and Downs (1979)
used unarmed sepals as diagnostic for subgenus
Macrochordion. Wendt (1997) discussed a close re-
lationship between Aechmea subg. Macrochordion
and some Brazilian species of subgenus Pothuava
(A. alopecurus, А. brueggeri, A. guarapariensis, A.
ornata, A. pineliana) based on their simple strobi-
late inflorescences, but that putative relationship
appears equivocal here.

CLADE 8

This clade consists of the two species sampled
from the genus Ronnbergia (Fig. 1). Like Strepto-
1979)

acks petal appendages. Three synapomorphies de-

calyx, Ronnbergia (sensu Smith & Downs,

—

fine the clade (characters 6, petiolate leaf blades;
7, leaf margins with less than five spines; 10, chan-
neled false midrib), though only the first character
is without homoplasy. Ronnbergia is a small genus
of 11 species characterized by a strong geographic
disjunction. Eight species have distributions re-
stricted to Central America and adjacent north-
western. South America (Colombia to Ecuador),
where they probably originated (Benzing, 2000).
The remaining species (Pereira & Penna, 1985;
Martinelli & Leme, 1987; Leme, 1999) are endemic
The Ronn-

to northeastern Brazil in Bahia State.

Volume 91, Number 2
004

Faria et al. 313
Cladistic Relationships of Aechmea

bergia clade received moderate support (bs. 69%);
however, the three Brazilian species were not sam-
pled in this study, implying monophyly for the non-
Brazilian part of the genus. Benzing (2000) argued
that this pattern of geographic disjunction exhibited
by some Bromelioideae might suggest erroneous
systematics rather than more recent
long-distance dispersals. Conversely, Leme (1999)
has suggested that the Atlantic Rain Forest flora of
northeastern Brazil has been deeply influenced by
the Amazonian flora, and thus the presence of
Ronnbergia in Brazil is not unexpected. However,
Leme (1999) did stress that new investigation must
be done to elucidate the natural placement of these
three Brazilian Ronnbergia species compared with

ancient or

Aechmea.

CLADE 9

Streptocalyx floribundus, Aechmea lingulata
(subg. Aechmea), and A. burle-marxii (subg. Ortgie-
sia) form a clade that holds these taxa sister relative
to the remaining ingroup (Fig. 1). The relationships
between A. lingulata and A. burle-marxii received
good support (bs. 85%): however, with S. floribun-
dus the clade is unsupported and defined by the
homoplasious synapomorphies: long inflorescences,
greater than 30 cm (character 19) and lax dispo-
sition of the flowers on the inflorescence branches
(character 22). These results agree with Smith and
Spencer (1992), who reduced Streptocalyx (sensu
Smith & Downs, 1979) under Aechmea, arguing that
the occurrence of petal appendages by itself is not
enough to delimit Streptocalyx as a distinct genus.
The validity of the presence versus absence of petal
appendages as the sole character for generic delim-
itation was first questioned by Brown and Terry

(1992). According to them, petal appendages are
the last structures formed in the flower, represent-
This kind of

character may be more susceptible to evolutionary

ing terminal ontogenetic characters.

change because a modification or reversal in such
a terminal character will not affect preceding de-
velopmental steps (Sachs, 1982). For bromeliads,
Brown and Terry (1992) argued that petal append-
ages can be lost and/or gained repeatedly without
affecting the development and function of other flo-
ral organs and that homoplasy may be realized
more easily and without impact on the ontogeny of
earlier formed, nonterminal characters.

TAXONOMIC IMPLICATION

The results, while somewhat provisional, offer
the first explicit demonstration, with few exceptions
(1.е.. Aechmea subg. Chevaliera and Macrochor-

dion), that the subgenera of Aechmea do not oth-
erwise correspond to monophyletic groups (Fig. 1).
Therefore, the proposals of Smith and Kress (1989,
1990) to elevate all Aechmea subgenera (sensu
Smith & Downs, 1979) to generic rank are not sup-
ported. The morphological characters traditionally
employed in generic and infrageneric delimitations
within Bromelioideae display high levels of homo-
This degree of character ho-

—

plasy (see Table 3).
moplasy, in concert with the various emphases
placed on different characters, is likely to be the
reason for the divergent previous classifications
proposed within Bromelioideae. Presumably the ra-
diation of Bromelioideae into many diverse, even
physically extreme environments, invoked a mul-
titude of abiotic and biotic pressures that resulted
in certain attributes arising independently several
times (Terry et al., 1997). Many aspects of vegeta-
tive structure and function are homoplasious, as are
most of the many pollination syndromes recorded
for the family (Benzing, 2000).

The phylogenetic hypothesis presented here in-
dicates that traditional generic and subgeneric de-
limitations in Bromelioideae need serious reconsid-
eration. However, as indicated earlier, these results
best represent a first approximation, provisional in
nature, and do not merit any reorganization or no-
menclatural action. We are actively expanding both
the taxon and character samples presented here,
and augmenting these with DNA sequence data to
develop a more robust phylogenetic analysis of
Aechmea and related genera within Bromelioideae.

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cine. Hafner, New

-
— —

APPENDIX 1. 0 characters and states used
in the cladistic analysis

1. Mature leaf length: О = short leaves, to 50 c
leaves over 50 to 100 cm; 2 = very p leaves, over
100 cm. Bromeliads typically consist v as ste
bearing alternate, closely placed, leaves. The len th
of mature leaves provides an accurate indication of
rosette size.

. Blade па, O = not differentiated or only
slightly sc = differentiated.

. Number of leaves per rosette: 0 = more than 15; 1

to 15;

N

w

an vary gre atly within
re MU xd to the size of the plants (i.e., not all smaller
plants produce fewer leaves, and vice versa). This
character needs to be scored from living plants, before
the vouchers are prepared.

Volume 91, Number 2 Faria et al. 315
2004 Cladistic Relationships of Aechmea

їл

-

eo

©

=

دن

Leaf ornamentation: 0 = absent, leaf blades uniformly

sreen; | = present. Leaf color is exceptionally vari-
able and vivid among bromeliads, € often ла
trichomes. Several species are distinguished by ir

ular blotching or cross-banding pateras
Alteration in leaf color during anthesis: O = yes; 1 =
по. baie баг of leaf ornamentation, some es dis-
ange in leaf color during anthesis presum-
у to үкө in pollinator attraction. baa Шу, the
calor change increases toward t er of the ro-
elte, e.g., Aechmea recurvata; ы. the color
change ен the distal end of leaf blades, e.g.,

Leaf form: 0 = linear; 1 = petiolate; 2 = filiform.
Most Bromelioideae have linear leaves. Petiolate
blades (blade strongly narrowed at base), similar to
that of some dicots, and filiform eave (with narrow,
involute blades) are found in such genera as Ronn-
bergia and Acanthostachys, respect tively.
Leaf margin: O = spines more than 3 mm long; 1 =
to 3 mm.

Number of spines per 5 cm length of margin (at the
leaf middle point): О = 5
2 = 10

› spines or less; = 6109;

—

or more. Leaves with armed margins char-
acterize most Bromelioideae, and the length and den-
sity of these spines are variable within and between
genera.
Leaf apex па (excluding terminal spine):
acute; | = rounded: 2 = retuse; З = long-attenuate.
The leaf apex for Aec -— aus
great variation with the more common types being
acute and rounded. Redi plant develapment we ob-
served that leaf apex shape could ‹ 'hange. Young
plants may have
le: е, while latter ones will have a rounded apex,
e.g., Aechmea nudicaulis. Here only mature leaves
moe from the middle part of the rosette were
scored.
A false midrib: O = absent; 1 = slightly to strongly
channeled. Leaves may Ls sess a mid-longitudinal re-
gion thickened by a succulent, multiply layered hy-
padsemis: A 1 Talse midrib is commonly as-
soc а with the genus Ronnbergia, as petiolate
blac
Phillies О = spiral; 1 = distichous.
Scape: 0 = erect and exc eng the rosette; 1 = pros-
trate or slightly curved; 2 = erect ein short (hidden
in the center of the rosette). Der scapes are more
common in those genera analyzed except for Billber-
gia, where prostrate scapes are present in most spe-
cies. Very short scapes eee in the center of the
rosette characterize the outgroup Cryptanthus, but
may also be found in some, КОО Aechmea,
Ronnbergia, and ا‎
Scape bracts: 0 = imbric "kh excee ding the internode
he scape; | = not imbricate,
shorter than internode do leaving the scape e
sed.

ze
е
=
©
<
%
=
=)
2
—
Q
=)
=
^
>
=
—

pos

Se Scape bract diffe pega into sheaths and blades: О
= differentiated;
bracts resemble leaves, we a distinct sheath and
blade can be recognized.

Scape bract ү 0 = entire; | = эй
Scape bract color: 0 = green or pale gree fy = rose
or red. Freque {лге show colo | scape
bracts, which can help in pollinator attraction and

differentiated. Some scape

c
#2]

—

N

=

N

N

w
+

w

ven seed dispersal when they remain brightly col-
a after the flowering period.

Scape bract texture: 0 = coriace 1 = membra-
naceous or chartaceous. Usually зде liad leaves
are coriaceous and some scape bracts show similar

Scape bract apex (excluding the terminal spine): 0 =
acute; 1 = rounded; 2 = long attenua

Inflorese ‘ence length, excluding the Meer sc تي‎ (em):
0 = to 10; 1 = over 10 to 30

=

› 30; 2 = over 30. Except
js the oe species, where inflorescences never
eed a few centimeters, this character varies greatly
within and among the genera analyzed. For individ-
uals that show great variation in this character (e.g...
Aechmea multiflora and A. sphaerocephala have inflo-
rescences that elongate as anthesis proceeds), an av-
erage was taken of at least two specimens observed
in different flowering stages.
Inflorescence rachis color: 0 = white, green, or rac his
color not visible (covered by congested flowers);
rose or red.
Inflorescence ty
|

—

c

ype: 0 = simple (racemes or spikes);

= once branched; 2 = two or more times ande hed;
3 — corymbose shape (simple or branch
Flower TS congela d on rachis or d 'ence васе h-

—

es = — yes.

Flowe Br arrange ment along the rachis or inflorescence
branches: 0 = polystichous; 1 = distichous.

Primary buck | absent; | = present. Branched

inflorescences have one Iu at the base of each
branch. The primary bra the one present in the
lowest or first branching. Simple inflorescences do not
ауе a primary bract.

Primary bract margin: 0 = armed: 1 = entire. If pri-
mary bracts are absent, characters 25—28 were coded
as inapplica

—

Primary е E О = greenish or pale; 1 = yellow
or orange; 2 = rose or red.
Primary bract texture: О = coriaceous: 1 = membra-

Primary pi apex: “we acute; 1 long attenuate:
= rounde
Floral biralar О = present; | = absent. Floral bracts

are characteristic br most Bromelioideae and they
can vary from much reduced (e.g..
Lamproc occus) to well developed, sometimes ехсее‹
ing the flowers (e.g., Aechmea subg. Chevaliera).
Floral bract margin: ce = entire; 1 = armed. If floral
bracts are absent, пани 30-37 were coded as
а “able.
Fk

ral braet color: O green, pale green, or casta-

neous; | = yellow or orange; 2 = rose or red; 3

b mm i or r purple.

Flor: al bract texture: О = membranaceous or charta-
ceo = coriaceous or fleshy.

Floral bract apex geni terminal spine): 0 =
rounded; 1 = long- attenuate; 2 = acute.

Terminal spine in the apex ol the floral bract: О =
absent or much reduced; 1 = present, but shorter

than the bract; 2 — e qualing or longer than the bract.
The majority of d spin analyzed have floral bracts
with terminal spines. These spines can be very short
(Billbergia) or we " pg eyar) sometimes being lon-
ger than the bra

Floral brat shape . ratio): Ө = broadly
ovale (1: y broadly ovate (1:2); 2 = nar-
rowly duxi 3:1); * = ovate (2:1).

316 Annals of the
Missouri Botanical Garden
36. Floral bract carinate: 0 = no; | = yes, l keel; 2 = blue, lilac, or pur; ple; 2 = red or rose; 3 = yellow
2 or 3 keels. orange; 4 = bicolored: mostly white, yellow, or green,
37. Shape of floral bract relative to the flower: О = flat; and the apex blue.
| = concave (enfolding ovaries, sepals, and some- 48. Petal apex: 0 = rounded; | = acute; 2 = retuse.
times the whole flower). Concave floral bracts may 49. Petal shape: 0 = linear; y — spatulate.
occur in many Bromelioideae taxa and are frequently 50 4 tal sin ndage: 0 = absent; | = pouch- or sac-like;
related to the bract yat as broadly ovate (1:1) and ringed; 3 — кые. Some flowers possess
very broadly ovate E 2). Bracts enfolding only the tissue outgrowths on the adaxial surfac
vary or most of the « are the most common con- called petal appendages. Petal appendages are absent
dition (e.g., Aechmea bromeliifolia) in Streptocalyx, Fernseea, Ronnbergia, and Cryptan-
38. Flower le ah (without the pedicels ): О = less than 2 thus (outgroup
emi ] = = 2 to 3.5 cm; 2 = over : 5 em. 51 ‘la en lateral folds on the adaxial surfac e: 0 =
39. Pedicel: 0 = absent; 1 = = pres ‚ In Aechmea, ped- = present. Some petals present OA
icellate flowers are found in a Podaechmea ole like outgrowths « al d late ral folds that can oc-
and some species of Lamproc occus. For other genera cur independently of the 5 of petal append-
pedicellate flowers characterize Portea and Fernseea. ages, i.e., Aechmea subg. Chevaliera, or in combina-
Flowers without a pedicel are more common within tion with them, ie., Billbergia. Except for
the subfamily. Hohenbergia, in most species analyzed the presence
40. Flower indumentum: 0 = absent; 1 = sparse with of lateral folds was related to the presence of petal
surfaces remaining visible; 2 = dense (pilose or lan- appendages. The oe pon nus does not possess
e) completely concealing the epidermal surfac- T Pl appendages or die f ү i
es. Most species analyzed present sparse indumentum ? pa a anthesis: LE erect or la * ri
covering floral structures. Dense indumentum char- bon . ole di € Гени are rus
Я scie «
acterizes Aechmea subg. Macrochordion, some species served for most species sampled and are constant tor
> aie Aechmea subgenera Macrochordion and Chevaliera.
of subge nus Pothuava, and genus He o henbergia. These à :
| 70 Spreading petal esent in some species of Ques-
species show lanuginose inflorescences, and this :
NA nelia, Lymania, Acanthostachys, Streptocalyx, am
characteristic is maintained dde in cultivation and " 4 :
the field Ronnbergia, bei onstant for Cryptanthus (out-
a ` roup). Recurved petals are a remarkable character-
Al. Sepal color: ( white, green, or pale green; 1
: istic for Billbergia.
blue, € ‚ ог de = red or rose; З = yellow or . " : T
53. Ovary cross section: 0 = terete; 1 = trigonous; 2 =
orange; 4 = bicolored, frequently green- -toned with a
laterally al sana
dad colored tip. E Е E ,
. 54. Ovary surface smooth; 1 = finely verrucose; 2
42 yal apex: O = rounded; | = "E = longitudi al Ne
43. Terminal spir x of | sepals: ( absent or = longitudinal furrows.

н 1 i ы EI. p | | | n ‘ 55. Ovary color: 0 = white or green; ellow or or-
жез рари исе‹ = 9 resent, m 8 on rt 2" p se- ange; : > or red: 3 = blue, lilac. ‚ ог purple
5 gr ing o exceeding ine жш ^ a ' 56. Filament shape: 0 = complanate; 1 = filiform

without apical spines occur in a few Bromelioideae 57. Filament adnation to petals: 0 = adnate Es m. ней
(Quesnelia, Aechmea subgenera ае rochordion, Lam- ment: 1 = adnate above mid-filament: iont
prococcus). pical spines can very short to well free (adnate for less than half of the 1
developed. sometimes longer idu the sepal length 58. Types of p n | grains: 0 = ina Vei gen e = sulcate;
iis last characteristic (2) is present in most of Aech- 2 = 2 pores: 3 = 3 pores; 4 = :5-250
mea subg. Ortgiesia and in some species of subgenus more pores. p species are ‘polymorphic for his
> o
Pothuava. character with more than one type in the same anther
44. Sepal symmetry: 0 = symmetric or slightly asymmet- (see Appendix 2). This occurred in different genera
ric; | = strongly asymmetric. Most Aechmea and re- sg. Acanthostachys, Streptocalyx, Hohenbergia, and
lated genera possess a lateral wing on sepals making n Aechmea subg tyaechmea). For the outgroup
them strongly asymmetric. (Cryptanthus), inaperturate grains are characteristic.
45. Sepals carinate: О = yes; | = no. 59 bit: 0 = ob Der terrestrial or saxicolous; | — fac-
46. Sepal connation: 0 = free; 1 = connate by 1/3 or ultative epiphyte
more of its length. 60 bias tte e a water impounding tank: 0 = no; |
47. Petal color: 0 = white, cream, or pale green; | = ye

317

Faria et al.

Cladistic Relationships of Aechmea

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Botanical Garden

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319

Faria et al.

Volume 91, Number 2

2004

Cladistic Relationships of Aechmea

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WHAT IS THE TAXONOMIC
STATUS OF POLYGONELLA?
EVIDENCE OF FLORAL
MORPHOLOGY '

L. P. Ronse De Craene,? S.-P. Hong,” and
E. F. Smets*

ABSTRACT

A Gom param pesi tenir val study of floral characters of the North Ален an genus Polygonella and the four
ct. P )

ds accepted sections of Polygonum s. str. (se

been carried out with light microscopy (1

=
=
a
Lp
А
^
*
=
=
=
=
=
=
9e
A
=
=
=
2
=
-
E
=
3
=
e
Y.
2
А
=
—
=

sect. sect. Pseudomollia, sect. Tephis) has
SEM

‘lowers were investigated for

mac ase al characters, tepal epidermal characters, pollen, and fruit morphology and anatomy. Results dem-

onstrate that the limits between both

enera become blurred through section Duravia of Polygonum, especially

in

characters of pollen and fruit morphology. Polygonum sect. ен and Polygonella share a wealth of intergrading
I 8) 8 807

floral and vegetative characters 1acroscopic, as well a

flower structure, vegetative 1 These characteristics, especially the pollen morphology

from section Polygonum. Evidence presented here allows

ultrastructural, level (pollen кард fruit morphology,
are sharply delimited
і

for a broader concept of Pm s. str. to be adopted,

with an extended section ins ia including subsections Duravia and Polygonella. A cladistic analysis of morphological

characters supports two distir
with subsections Duravia 5 1 lla.

Key words: cladis
sectional classification.

clades, section Polygonum with subsections Polygonum and Tephis, and section Duravia
yg YS

tic analysis, Duravia, floral morphology, fruit, pollen, Polygonaceae, Polygonella, Polygonum,

The genus Polygonella Michx. contains about 9
to 11 species native to eastern North America, with
a few western outliers. The genus was originally
erected by Michaux in 1803 to accommodate a sin-
gle species, P. parvifolia Michx. Since that date a
number of North American genera were described
n for the Polygonaceae. Fischer and
Meyer (184 iii desc ribed the genus Gonopyrum
Fisch. & s ‚ А. M

americanum).

ey. with one species (G.
1 described several new
genera in the Polygonaceae, which were eventually
transferred into Polygonella, such as Lyonia Rafin.
(1808: 352), Phyllepidum Rafin. (1808: 356), Ly-
onella Rafin. (1818: 266), Phylepidum Rafin.
(1836: 51), and Stopinaca Rafin. (1837: 11). Gray
(1845: 232) recognized the genus Thysanella with
one species (T. fimbriata) originally placed in Po-
lygonum. Nieuwland (1914: 171) created the genus

P. articulatum
Nieuwl. and P americanum Nieuwl. Small (1896,
1909, 1913, 1924) described five new species in
Polygonella and erected two additional genera (De-
lopyrum and Dentoceras). In 1933 he recognized 13
species under four distinct genera (Polygonella,
Delopyrum, Dentoceras, and Thysanella A. Gray).
while absorbing the other previously described gen-
era. However, all were included by Horton (1963)
under Polygonella, because he considered the dif-
ferences used by Small (1896, 1909, 1924)
regate these smaller genera not distinctive enough.

Psammogonum for two species,

to seg-

The arguments used by Horton (1963) to recognize
a single genus were mainly the homogeneity in
anatomy and flower form against the heterogeneity
in the neighboring genus Polygonum, although his
views of the latter genus were doubtless much

broader than in the present paper. An additional

! We thank I.
unpublished MSc. thesis at our disposal. We thank Peter
latum.
ac knowledged. This 5
and project n? 6.0143.

from the Korea Research Foundation and a *

? Royal Botanic Garden Edinburgh, 20A
l.ronsedec ‘raene@rbge.org.u

3 Laboratory of Plant $
130-701, Korea. sphongOkhu.ac.

' Laboratory of Plant

C. Oh (Kyung Hee University, Seoul) for kindly putting part of his photographic material from his
Linder for sending Р material of dial unda
Technical assistance by Anja Vandenperre for material studied at о (Ка
was supported by research grants (project n°
; general research project from the F. M. O.).
(OT/97/23) to L. Ronse m Craene, and by research grants (Non-Directed Research Fund: Project n°

holieke Universiteit Leuven) is
38. 91: scanning electron microsc "n
a grant ак the Research а il of the

)1-001 - n

D

3 Professor Sabbatical Year’ from Kyung Hee Universi to S.-P. Hong.
The following herbaria are acknowledged E: the use of specimens: BOL, BI 1
Inverleith

1, E, K, LV, NY, S, UPS.

How, Edinburgh EH3 2 R, Scotland, U.K

Syste mali 8, a epaine nt of Biology & Institute of Basic Sciences, Kyung Hee University, Seoul

EM Institute of Botany and Mic ee Katholieke Universiteit Leuven, Kasteelpark

Arenberg ЗІ, B-3001 Leuven, Belgium. erik.smets@bio.kuleuven.ac.

ANN. MISSOURI Bor.

GARD. 91: 320—345. 2004.

Volume 91, Number 2

Ronse De Craene et al.
Taxonomic Status of Polygonella

argument already used by Small (1897) is the fact
that branching in Polygonella is internodal by ad-
nation of the secondary axis to the main axis above
a node, contrary to other members of the Polygon-
aceae. Eleven species are currently recognized. For
population size and distribution we refer to Lewis
and Crawford (1995). Horton (1963) did not con-
sider the generic limits of Polygonella, nor did he
make comparisons with taxa outside the genus.
Meisner (1857) related Polygonella with Atraphaxts
L. in a separate subtribe. Only later did authors
consider it as related to Polygonum sensu lato
(Bentham & Hooker, 1883; Dammer, 1893), al-
though always as a distinct genus.

The most important distinctive characters of Po-
lygonella enumerated in the literature are that the
branches appear internodal by the fusion of their
basal part to the main stem, the abruptly dilated
inner filaments, the presence of solitary flowers on
elongated. pedicels at the nodes, the colored mar-
cescent tepals, and conspicuous scarious bracts
(Watson, 1873; Small. 1897; Rydberg, 1932: Gra-
ham & Wood, 1965; see Table 2). Horton (1963)
added a few anatomical features, such as the very
short vessel elements and a strongly reduced. vas-
cularization of the flower (as was observed by Vau-
tier, 1949).

Horton recognized two subgenera in Polygonella,
viz. subgenus Polygonella comprising the great ma-
jority of the species, and subgenus Thysanella with
only one species (Polygonella fimbriata (Ell.) Hor-
ton) consisting of two varieties. Subgenus Polygo-
nella was described as having two outer and three
inner morphologically distinet tepals, pedicels
without bracteoles within the ocreolae, and fila-
ments that are dilated at the base, forming two lat-
eral teeth. Subgenus Thysanella has two outer, one
transitional, and two inner tepals, pedicels sub-
tended by bracteoles within the ocreolae, and the
filaments all alike and without teeth. Nesom and
Bates (1984) considered the two varieties of Poly-
gonella fimbriata as two valid species, P. fimbriata
and Polygonella robusta. In a cladistic analysis,
Lewis (1991, cited in Lewis € Crawford. 1995)
found that P. fimbriata and P. robusta appear as a
basal clade within Polygonella.

The circumscription of the genus Polygonum L.
has changed considerably since its much broader
circumscription by earlier authors. In recent ap-
proaches to the family Polygonaceae, the genus is
currently segregated in the genera Polygonum s.
str., Fallopia Adans., Persicaria Mill., with segre-
gates Aconogonon (Meisn.) Rchb. and Bistorta
Mill., and Koenigia L. (e.g.. Haraldson, 1978;
Ronse De Craene & Akeroyd, 1988; Brandbyge,

1993). Four sections are currently accepted within
Polygonum s. str. (e.g., Dammer, 1893; Hedberg,
1946:
lia, Tephis, Polygonum (= Avicularia). and Duravia
(see Table 1).
(1988)

Tephis), as they believed the distinctive characters

Haraldson, 1978), viz. sections Pseudomol-

Ronse De Craene and Akeroyd

recognized two sections only (Polygonum,
| yg

to be unimportant in comparison to the inherent
variability of section Polygonum. Haraldson (1978:
79) summarized the differences between the tribes
of Polygonum s. str. in a table. She reported the
presence of three staminodes besides five fertile
stamens as a distinctive character for sections
Pseudomollia and Duravia. Watson (1873) and Har-
aldson (1978) pointed out that section Tephis is
more similar to section Duravia than to section Po-
lygonum.

Section Duravia was erected by Watson (1873)
for a single species, Polygonum californicum, on
the basis of its supposedly distinctive achene struc-
ture (with a membranaceous pericarp). Small
(1895) included four other species in his subgenus
Duravia (Polygonum bolanderi, P. greenei, P. par-
ryi, P. bidwelliae) on the basis of lacerate ochreae
and spicate inflorescences. Greene (1904) elevated
Duravia to generic rank on the basis of three dis-
tinctive characters (viz. solitary flowers, persistent
styles, and absence of articulation at the base of
the leaf blade). He accepted three other species (D.
bidwelliae, D. greenei, and D. bolanderi) besides D.
californica.

The taxonomy of North American Polygonum.
sections Polygonum and Duravia alike, remains
confused, as different populations tend to show
wide gene flow and a high level of interbreeding
e.g. Mertens & Raven, 1965; Wheeler, 1938).

Hickman (1984) tried to solve this problem by ac-

—

cepting two polymorphic species, Polygonum po-
lygaloides and Polygonum douglasii, each with a
number of subspecies that had been previously de-
scribed under various species. He elevated section
Duravia to the rank of subgenus with two sections,
section Duravia with five species and section Mon-
ticola with the two heterogeneous species.
Hedberg (1946) described a distinct pollen type,
the Duravia-type, for 18 species of Polygonum sen-
su lato, deviating from the other species of the ge-
nus, and including members of Polygonella. How-
ever, several species possessing the Duravia-type
of pollen were placed by Small (1895) in his sub-
genus Avicularia (equivalent to sect. Polygonum).
Based on the study of a limited number of species,
Haraldson (1978) recognized section Duravia as

distinct from section Polygonum by its petiole anat-

322 Annals of the
Missouri Botanical Garden
Table 1. Summary of the most important delimitations of Polygonum s. str. and Polygonella (full line

indicates that certain sections were not considered by the authors).

&
Hooker (1883),

S
Meisner (1857) Dammer (1893) (1895,

mall

1933) Gross (1913) Jaretzky (1925)

Sect. Avicularia Sect. Avicularia

Sect. Avicularia Sect. Pseudomollia —

Sect. Avicularia Sect. Avicularia
Sect. Tephis Sect. Tephis

Polygonella Polygonella

Subg. Polygonum

Subg. Duravia

Polygonella, Dento-

Sect. Avicularia Avicularia sect. Avi-

cularia
Sect. Avicularia Avicularia sect. Avi-

cularia
Sect. Avicularia Avicularia sect. Avi-

ularia
Sect. Tephis Avicularia sect. Te-
phis
Polygonella Polygonella

ceras, Delopyrum

Thysanella

omy and found it anatomically closer to Polygonella
than to section Polygonum.

Other authors did not recognize the identity of
section Duravia, mainly because of the observed
existence of transitional forms between section Du-
ravia and section Polygonum (see Dammer, 1893;
Gross, 1913; Jaretzky, 1925; Graham & Wood,
1965; Ronse De Craene & Akeroyd, 1988; T.
1). Several North American species were retained
in section Polygonum (Watson, 1873; Small, 1895),
or no difference was made at the sectional level
(Rydberg, 1932, 1954; Small, 1903, 1933; Kaul,
1986). Indeed, the taxonomy of section Duravia ap-
pears confusing and it is difficult to draw a sharp

Table

line between section Polygonum and section Du-
ravia, especially in the annual species of section
Polygonum. Polygonella, on the contrary, has been
maintained as a distinct genus by all authors de-
spite the fact that several distinctive features of Po-
lygonella are found in Polygonum s. str., especially
in the species that have been grouped under sec-

tion Duravia. These characters include:

@ The presence of a single unbranched vein in
each tepal (Vautier, 1949; Horton, 1963; Graham
& Wood, 1965; Ronse De Craene & Akeroyd,
1988);

@ The corresponding vegetative anatomy of section
Duravia and Polygonella (Haraldson, 1978);

€ The lateral expansion of the (inner) filament ba-

s does not occur in all species of Polygonella.

In Polygonella fimbriata filaments are basally in-
ated as in Polygonum sect. Polygonum and
section Duravia; the inner filaments of Polygo-
nella macrophylla are intermediate (Horton,

1963)

ө The similar epidermal cell morphology of the te-

pals no De Craene & Akeroyd, 1988; Hong
et al.,
e The a as of Polygonella and Pc
lygonum sect. Duravia appears | to be ен
(Hedberg, 1946; Nowi Skvarla, 1977;
Hong & Oh, Hedberg (1946)

found four species of Polygonella matching the

icke
unpublished).

pollen grains of Polygonum sect. Duravia (*Du-
ravia-type"). However, he found one species, Po-
lygonella parvifolia (= Polygonella polygama),
that had pollen grains almost identical to section
Polygonum (“Avicularia-type”), but he was not
convinced of a close relationship, as important
differences exist in habit and phytogeographical
distribution. He concluded that there had been
development of the same pollen type in

—

paralle
the two groups.

The apparent trend for the outer stamens to be—
come reduced or lost (a reduction of the total
from eight to three; see also Ronse De Craene &
Akeroyd, 1988); this trend is correlated with an
expansion of the inner filament bases and occurs
occasionally in Polygonella (Horton, 1963), Po-
lygonum sect. Duravia (Wheeler, 1938), and sec-
tion Polygonum (Trail, 1896; Ronse De Craene
& Akeroyd, 1988). Gross (1913) mentioned one
Polygonella po-

case of Pol ygonella parvifolia (=
lygama) with five stamens: three inner, and two
outer (replacing the two pairs). An identical dis-
position is occasionally found in Polygonum
sect. Polygonum (Vautier, 1949),

Ronse De Craene and Akeroyd (1988) briefly
discussed the possibility of combining Polygonella
and Polygonum s. str. into a single genus. In this
paper we provide arguments for solving the prob-
lem, as more evidence has been gathered from dif-

Volume 91, Number 2 Ronse De Craene et al. 323
2004 Taxonomic Status of Polygonella
Table 1. Extended.
Ronse De Ronse De
Haraldson Craene & Craene & Hong

Hedberg (1946)

Graham &
Wood (1965) (1978)

Akeroyd (1988) (as proposed herein)

Sect. Polygonum Sect. Polygonum
Sect. Pseudomollia —
Sect. Duravia Sect. Polygonum
Sect. Tephis —

Polygonella, Gono- Polygonella subg.
pyrum
Thysanella

Thysanella

Sect. Polygonum
Sect. Pseudomollia
Sect. Duravia
Sect. Tephis
Polygonella

Polygonella
Polygonella subg. —

Sect. Polygonum Sect. Polygonum sub-
sect. Polygonum

Sect. Polygonum Sect. Pseudomollia

л

ect. Polygonum Sect. d sub-

. Duravia

Nn

ect. Tephis a ым sub-

sect. fephis

Polygonella subg. Sect. Duravia sub-

sect. о нен
. Dure

sect. 5

»onella

n

Polyg
Rl subg.
Thysanella

ferent fields. The limits between the sections Pseu-
domollia, Tephis, Duravia, and Polygonum, relative
to Polygonella, are also studied and clarified.

MATERIAL AND METHODS

A number of representative species of Polygo-
nella, and species from all sections of Polygonum
Tephis, Pseu-

Сив and Polygonum, have been investigated.

Nn

str., including sections Duravia,

Material was either fixed in the field in FAA
removed from herbarium sheets. The origin of ma-
terial is listed in Appendix 1. We studied selected
characters considered to have systematic value
based on previous studies, viz. pollen (Hedberg,
1946), fruit anatomy and surface patterns (Marek,
1954, 1958; Wolf & McNeill, 1986; Ronse De Cra-
ene et al., 2000), tepal epidermal structure (Ronse
De Craene & Akeroyd, 1988; Hong et al., 1998),
and gross floral morphology (Ronse De Craene &
Akeroyd, 1988).

For LM observations herbarium material was ei-
ther boiled in water or treated with sulfosuccinic
acid 1,4-bis ester sodium salt (aerosol-OT: Ayensu,
1967). Flowers were first washed in a warm 10%
KOH solution,

bleach was applied to remove the excess of tannins

before a treatment with Stockwell's

(Schmid, 1977). Next material was run through an
ethanol-tertiary butanol series and embedded in
paraplast, sectioned at about 12 um, and stained
with saffranin and fast-green. The vasculature of a
number of flowers was also studied after treatment
with warm 10% KOH and clearing with lactic acid
(Sporne, 1948).

the fruit wall only the exocarp (epidermis)
survives at maturity and is usually lignified. As the
cells are square, rectangular, or cylindrical they

have the same shape in cross or longitudinal sec-
tion. However, tangential (paradermal) sections can
vary from the epidermis toward the mesocarp. In
surface view the cells may be puzzle piece- to star-
shaped, and become polygonal deeper within the
2000).

For SEM observations herbarium material was

tissue (see also Ronse De Craene et al..

treated with aerosol-OT, stored in 70% alcohol (Er-
bar, 1995), and dissected before treatment with di-

and

—

methoxymethane (Gerstberger & Leins, 1978
critical-point drying. SEM observations were car-
ried out either with a Jeol 6400 scanning electron
microscope (LV) or Zeiss DSM 962 (E) at 5-15 kV.

We also studied a number of observable macro-
morphological features of leaf, stem, inflorescence,
and mature flowers and fruits, such as the overall
shape of the flower, the shape of the tepals, tepal
venation, the number of stamens and the filament
shape, the number of carpels, and shape of the
fruits. These characters were added to the micro-
morphological characters to perform a cladistic

analysis comprising 51 characters and 25 species

—

(including one subspecies) (see Appendices 3, 4
Parsimony analysis was performed with PAUP* ver-
sion 4.0 (Swofford, 1998)

Fallopia cilinodis (Michx.) Holub was used
outgroup, and characters were unordered and all
had equal weight. Polygonum molliaeforme was ini-
tially included in the analysis, but was later re-
moved because of strong morphological conver-
gences (see discussion). Parsimony analysis was
performed using a heuristic search with TBR swap-
ping and the steepest descent option. Relative sup-
port for clades was assessed with a 50% majority-

rule bootstrap and jackknife analysis.

Annals of the

324

Missouri Botanical Garden

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Volume 91, Number 2

Ronse De Craene et al. 325

Taxonomic Status of Polygonella

OBSERVATIONS

—

MACROMORPHOLOGY OF THE FLOWER (FIGS. 1,2

All tepals are similar in size and shape (Figs.
1D. 2C. D. F).

from the inner ones (Fig. IA. C. E). In some cases

or the outer tepals differ strongly

shape and size of tepals became increasingly dif-
ferent after anthesis. Outer tepals were found to be
angular to keeled in species of sections Polygonum,
Duravia, and Tephis (Figs. 1А, E, 2D). In section
Polygonum the fruit tends to outgrow the perianth
in size as lo become increasingly exserted, and the
tepals become appressed to the fruit. In. sections
Tephis, Duravia, and Polygonella the perianth
loosely encloses the fruit, often becoming accres-
cent. A distinctive characteristic of some species of
Polygonella (e.g., Polygonella americana, Polygo-
nella polygama) is that the outer tepals become re-
flexed and are smaller than the accrescent inner

The vasculature of the tepals is only rarely trifid

(e. g.. Polygonum afromontanum; Fig. ТА). In most
cases it consists of a single dendritically branching
vein (as a main trunk with short secondary ramifi-
cations along the trunk: most species of section Po-
lygonum and some of section Duravia; Fig. 1B,
In Polygonella, Polygonum molliaeforme, and some
species of section Duravia there is only a single
non-branching vein, or ramifications are few (Fig.
IC, E)

The most common arrangement of the stamens
in the pentamerous Polygonaceae is of four equal
stamens in two pairs opposite the two outer tepals,
two unequal stamens opposite the intermediate te-
pal (one belonging to the inner whorl and one to
the outer whorl), and single stamens opposite the
two inner tepals (Fig. IB. C: see. e.g.. Laubengayer,
1937; Vautier, 1949; Ronse De Craene & Smets,
1991). Flowers are occasionally trimerous with six
tepals (Fig. 1D). The transitional tepals have an
intermediate shape and size (Figs. LA, B, 2С, E) or
are sometimes abnormally shaped (Fig. 1D). A sin-
gle stamen is often found in sections Tephis and
Polygonum molliaeforme instead of the usual sta-
men pair (Fig. 1А, К). Anthers are occasionally
sterile, as in Polygonum ramosissimum (see also
Ronse De Craene & Akerovd. 1988). In all taxa
studied the filaments of Шу: inner stamens are in-
flated toward the base (Figs. LA—E, 2A—E). In most
species, the inflation is basipetally progressive from

the middle of the filament, but in most species of

Polygonella the filament abruptly widens in the
lower half (Figs. 1С, 2A). However, this is not the
case in Polygonella fimbriata, and its outer fila-
ments are rarely inflated and are sometimes ге-

duced (Horton, 1963). Nectar tissue is confined to
the base of the inner filaments and extends onto the
hypanthium surrounding the ovary. The nectary is
not clearly visible, except for the epidermis that is
not cutinized. Since no nectarostomata are visible,
diffusion of nectar must take place through the non-
thickened cell wall (cf. Ronse De Craene & Smets,
1991). Only in one species, Polygonella articulata,
did we observe an apparently glandular rim (nec-
tary?) of tissue surrounding the base of the gynoe-
1963). For more details on
Ronse De

cium (see also Horton,
nectaries in Polygonaceae we refer to
Craene and Smets (1 ).

The shape of the gynoecium is either trigonous
(three carpels) or lenticular (two carpels). and the
fruit develops as an achene or nut. Á condition with
two carpels is consistently found in sections Pseu-
domollia (Vig. 6C) and Tephis, rarely in section Po-
lygonum, and is almost absent in section Duravia
and Polygonella. This may correspond with the loss
of the intermediate tepal with accompanying sta-
mens (Fig. 2D). Other differences between individ-
ual species exist in the presence (Figs. 6A, 7C. D)
versus absence (Figs. 6C, 7A, B. К) of a basal stipe.
the prolongation of the distal portion (beak) of the
achene (Fig. 7C—F), as well as the development of
the fruit angles or ribs (Figs. бА. B. 7B. D. F).
Fruits of Polygonella and several species of section
Duravia are typically slender, triangular-ovoid with
well-developed angles, stipitate, and beaked (Fig.
7C, D, К), although this is not always consistently
so (Fig. 7A, E). The fruit of Polygonum molliaefor-
me is distinctive by the presence of a winged beak
(Fig. 6C), although the wings may be variably de-
veloped. In section Polygonum the fruit is often
in transection, as two ribs are more
or the

disymmetric
prolonged compared to the third (Fig. OB).
opposite occurs (Fig.
POLLEN MORPHOLOGY (FIGS. 3, 4)

In all genera and sections investigated the pollen
is prolate to spheroidal and tricolporate (Polar axis/
Equatorial diameter = 1.11—1.68). The ektexine is
the most variable feature, and is either reticulate
(Fig. 3B-F, H, 1), tectate (smooth and spinulose:
Fig. ЗА). or rough (Fig. ЗС). In species with a re-
ticulate exine, usually the area surrounding the col-
pi features smaller lumina than seen in the polar
and intercolpal area

Species of ful со sect. Polygonum and sec-
tion Tephis (Avicularia-type sensu Hedberg, 1946)
consistently have tricolporate, rarely hexa-panto-
colporate (= hexarugate), prolate-spheroidal grains
with the exine surfaces smooth with spinules (Figs.

326 Annals of the
Missouri Botanical Garden

Figure l. Floral shapes and structures, with flowers spread open and gynoecium removed (О, outer stamen; I, inner
stamen; T, transitional stamen). —A. Section Tephis: Polygonum afromontanum (Danish-Ethiopian Bot. Exped. 1622).
—B. Section Duravia: Polygonum douglasii (Rydberg & Bessey 5364). —C. Polygonella polygama (Godfrey 1046). —

). Section Polygonum: Polygonum aviculare (Ronse De Craene 25 Lb). —E. Section Pseudomollia: Polygonum mol-
liaeforme (Bornmiiller 8181). A, bar = 0.6 mm; B, C = 0.5 mm; D = 0.3 mm; E = 0.4 mm.

Volume 91, Number 2 Ronse De Craene et al.
Taxonomic Status of Polygonella

|
Н

k
Р ў

- ^i T

Figure 2. F жа rs of Polygonum and Polygonella, SEM mic ee Ni Y Polygonella parksii: stamens and gynoe-
ll & Correll 36649). —B. dies ae wade lower spread open (Jepson
flower spread open

ygonum aviculare:
carp; Т,

E

cium; one inner tepal removed (Corre
|

C. Polygonum tenue: flower Polygonum dul uum:
Ll . Po

spre 'ad open Pulsa и s.n.).
flower spread open ns De Cr aene 25

An.

a 5962). — Polygonum aviculare:

transverse section of ove a De Craene 25 Lb). (E, embryo; 1, inner stamen; 0. n tame n; P, peri
Bars = ) рт. except С. D | mm

E tional. Pond n).

328 Annals of the
Missouri Botanical Garden

18 m

Figure 3. 5 view of pollen grains of Polygonum and о lla, SEM micrographs. —A. Polygonum

avic ware e хаг 15203). —B. Polygonum ae) Je 2 s.n.). —C. I Polygonum 7 5 var. latifolium (How-

ell s.n.). —D. ене e e (Kotschy 778). —E. Polygonella americana (Fischer 10). —F. Polygonum tenue

(P isan s.n.). —G. Polygonum * (He be rg 4320). —H. Polygonum minimum (Sandberg & Leiberg 799).
. Polygonella 1 (Godfrey 1046). Bars = 10 um

ЗА, ЛА). In Polygonum afromontanum the exine — mesocolpium, but mostly psilate around the ectoap-

surface is more or less roughened although com- — erture (Figs. 3D, 4D)
parable with section Polygonum (Figs. 3G, 4A). Several species of Polygonella (Fig. 3E) and of

Pollen of section Pseudomollia is tricolporate, Polygonum sect. Duravia (Figs. 3B, 3H, 4B) have
prolate, and nearly triangular in polar view (Figs. — tricolporate, prolate grains with a dimorphic exine
3D. 4D). It differs strongly from section Polygonum (Duravia-type sensu Hedberg, 1946). The exine is
in its dimorphic exine, verrucose on both poles and semitectate-reticulate at the mesocolpium and the

Volume 91, Number 2
2004

Ronse De Craene et al. 329

Taxonomic Status of Polygonella

P. afromontanum
do айги: polar vi Uo dass 4320). —RB. P cal-
ifornicum: detail of alveoli and mesocolpium (Jepson s.n.

—C. I ر‎ detail of alveoli around colpus (Sandberg

P. molliaeforme: d do гү. mesocol-
1 um

f Polygonum, SEM mira. —
ew

a

—

& баа rg (99). —

pium at ais and alveoli (Kotschy 778).

poles, and rugulate/reticulate or sometimes foveo-
late with microspinules around the ectoapertures.
For some (e.g.. Polygonella polygama, Polygonella
articulata, Polygonum en. Polygonum min-
Figs. 3C, F, I, 4C), the

the exine surface at ч mesocolpium and the ec-

imum: difference between
toapertures is a minor question of size, and is in
some cases not distinguishable (Fig. 31). Homoge-
neously distributed lumina are found in some Po-
lygonella (Fig. 31). As this difference increases.
.. Polygonum
Polygonella

distinction between

more typical Duravia-types occur (e.g
californicum, Polygonella атын.
americana: Fig. 3B, E). The
zones of reticulations may be abrupt (Polygonum
bolanderi) or progressive (Polygonum tenue: Fig.
ЗЕ). It is thus possible to construct a progressive
transformation series between the typical Duravia-
type with strict boundaries between the mesocolpal
area and the ectoapertural area and strictly retic-
ulate pollen with only a slight difference between
these zones.

TEPALS (FIG. 5)

EPIDERMAL CELLS OF THE

The adaxial epidermis of the inner tepals was
analyzed by Hong et al. (1998). We add more ob-
servations here that are in agreement with the pre-
vious results. Tepal epidermal characters cannot be
r. from Poly-

Two types of epi-

used to differentiate Polygonum s. sl
1998).

additionally be

gonella (cf. Hong et al.,

dermal cells can distinguished

herein (Fig. 5): more or less rectangular with

straight anticlinal walls (Fig. 5D). or puzzle piece-
shaped to rectangular outlines with undulate anti-
clinal walls (Fig. 5A-C. E). Cuticular striae are
mostly deep and randomly distributed, but some-
times aligned in one direction.

FRUIT MORPHOLOGY AND ANATOMY (FIGS. 6—9)

The value of fruit anatomy in Polygonaceae was
1922; Marek,

recognized previously (e.g.. Lonay.
1 1971) and has been used

954, 1958; Neubauer,
by us recently to delimit the tribes Polygoneae and
i 2000).

parameters have been recognized as taxonomically

Persicarieae (Ronse De Craene et al., Two
significant: (1) fruit surface patterns (with SEM)
(Figs. 6-8), and
and LM) (Fig. 9).

A single bitegmic seed develops from an ortho-

(2) pericarp anatomy (with SEM

tropous basal ovule and becomes surrounded by a
hardened pericarp. The pericarp consists of a seler-
ified exocarp, a mesocarp, and endocarp (see also
1922; Marek, 1958; 1971;
2000). The thickenings most com-

monly occur on the anticlinal (radial) walls. but not

Lonay, Neubauer, Ronse

De Craene et al.,

Annals of the
Missouri Botanical Garden

5.
Polygonum douglas 4 subsp. шша опис (Lyal 1858).
7).

arenastrum (Ronse De Craene 1157

on the inner tangential (periclinal) walls. As thick-
ening of the anticlinal walls increases from the in-
ner tangential wall to the outer, the lumen often
takes a triangular to trapezoid shape in section (Fig.
9B, E, F). i
more regular and e lumen appears narrowly rect-
angular (Fig. 9A,
branch from the hee into the surrounding scler-

In other instances the thickenings are
Jery often small canals
enchymatous tissue (Fig. 9A, B, H, I). Due to space
constraints the anticlinal walls can become vari-
ously convoluted or bent in cross or longitudinal
sections (Fig. 9A, C, 1). As convolutions of the an-
ticlinal walls may also occur tangentially, this gives
the cells a star- or puzzle piece-shape in surface
view or in paradermal section, or the cell appears
polygonal if no convolutions occur. Shifts in shape
may occur within the cells from the periphery to
1922).

of the epidermis represents interesting systematic

the mesocarp (cf. Lonay, The outer surface
characters, as emphasized by Marek (1954, 1958),
Wolf and McNeill (1986), and Ronse De Craene et
al. (2000).

In Polygonella the outer fruit surface is smooth

SEM micrographs of the inner tepal epidermis. —A. Polygonella parksii (Correll & Correll 36649). —B.

. Polygonum bolanderi (Pringle s.n.). —D. Polygonum

„. Polygonum иша. var. latifolium (Howell S. n.). Bars = 10 um

(Polygonella gracilis, Polygonella americana: Fig.
ТЕ, F), or with shallow pits (Polygonella articulata:
Fig. 8l).
present (Fig. 8I), but not in Polygonella fimbriata
(Figs. 7D, 8H), or in Polygonella gracilis. Polygo-
nella fimbriata has a mixture of a closely packed

Longitudinal cuticular striae are often

layer of "tubercles" on the upper fruit with a rough-
ly pitted lower surface (Figs. 7D, 8H). Smooth sur-
faces are also found in Polygonum sect. Duravia
(e.g.. Polygonum minimum: Fig. 7A, Polygonum
paronychia), and section Polygonum (e.g., Polygo-
num maritimum: Fig. 6A). In other species the up-
per half of the fruit can be tubercled and the lower
half smooth (e.g.. Polygonum oxyspermum subsp.
raul, Polygonum arenastrum), and this is related
with the pressure of the tepals at the base of the
fruit. Smooth surfaces with pits representing the
collapsed anticlinal walls of the cells were found
in sections Tephis (Fig. 8G), Pseudomollia, and Du-

ravia (e.g.. Polygonum shastense, Polygonum cali-

fornicum: Fig. 8D, Polygonum coarctatum, and Po-

aag)

8E). The

Polygonum polygaloides s.l. (including subspecies

lygonum tenue: Fig. fruit surface o

Volume 91, Number 2
2004

Ronse De Craene et al.
Taxonomic Status of Polygonella

Figure б. SEM
п (te pals removed).

877 iolliaeforme:

mic err of lateral views of entire
? maritimum: smooth surface
f sate
(He. dierg 132 20).

"Bar 100

kelloggti: Fig. ӨК: subspecies confertiflorum: Fig.
ТС) is unique and shows a scalariform-reticulate
pattern. with longitudinally running ridges bridged
at regular intervals with variations depending on
the samples or subspecies studied. These ridges do
not necessarily correspond with the anticlinal walls
of the cells.

Several species of section Polygonum and a few
of section Duravia have a distinct surface pattern
covered by tubercles. Tubercles may be equidistant
and sparsely covering the fruit along the anticlinal
walls of the cells (e.g., Polygonum bellardii: Figs.
6B, 8A), crowded on ridges formed by the anticlinal
cell walls (e.g..

Polygonum achoreum, Polygonum

with short apical wings (Kotschy

Molliaeforme,

? be M be rcled surface (Hek
|

fruits of d iaa a sects. Polygonum, and
(Nordin 102). —B.

778).

lreich

? afromontanum: pitted surface

equisetiforme: Vig. 8C). or in longitudinal rows or

clusters without. connection to the anticlinal walls

of the cells (e.g.. Polygonum arenastrum, Polygo-
num avic DRE ye вопит douglasii: Figs. ТВ, 8B).

Tubercles may be associated with pits. but never

with superficial striae. Polygonum douglasii and
Polygonum tenue differ markedly from most other
species of section Duravia in the presence of tu-
bercles arranged in short longitudinally placed
rows (Fig. 8B).

pitted surfaces and with globular emergences occur

In some cases fruits with smooth-
side by side in the same species (e.g.. Polygonum
arenastrum, Polygonum douglasii, Polygonum sper-

gulariforme, Polygonum kelloggii, Polygonum ten-

332

Annals of the
Missouri Botanical Garden

Figure 7. SEM micrographs of lateral views of fruits of i ales secl. Duravia and Polygonella.
I 8 E
l

minimum: smooth surface (Sandberg & Leiberg 799).
97 —(

722). ^.

gonella fimbriata: smooth surface, apically pitted (Blanton 682

sn). —E

ue: Fig. 8E).

liaeforme (sect. Pseudomollia) is distinctive with a

The lenticular fruit of Polygonum mol-

roughly reticulate surface and deep pitting along
the wings lining the beak of the fruit (Fig. 6C); the
reticulation is more compact and is covered with
tubercles at some places (see also Ronse De Craene
et al., 2000). The extent of development of the an-
gles of the fruit is correlated with a different surface
pattern between the ribs and the angles. In some
species this difference is well pronounced (e.g.. Po-
lygonella fimbriata, Polygonum molliaeforme: Figs.
6C, 7D

Polygonum polygaloides subsp. ** re tic icula Е surface (Bacigalupi & Smith

=

ү LI
P»
RU

15222
(far ewe
vs *

D)
D

EE

— pda q ni
jercled surface "m orter & Port
—D. Poly y-

Polygonum douglasii: tu

ce gracilis: smooth ыле (Vestulund
) uum

Polygonella americana: smooth to pitted surface (Ё Mm E Bars —

Sections of the fruit have been made for a rep-
resentative number of species (for details see also
Ronse De Craene et al., 2000). In LS the exocarp
consists of palisade-like cells (20-80 um thick)

with slightly undulate or straight radial walls. In

section Polygonum the radial walls appear convo-
lute because of irregular thickening on the inner
wall (Lonay, 1922; Neubauer, 1971).
rectangular with dendritical

The lumen of
the cells is narrowly
branching toward the outer tangential wall (Fig. 9A,
C). The wall is usually thick (> 60 jum) but some-
times thinner (< 40 рт as in Polygonum oxysper-

Volume 91, Number 2 Ronse De Craene et al.
2004

Taxonomic Status of Polygonella

Кк eric.

ш 8. SEM microgri p y A tails of fruit surfaces Bd Polygonum and Mis. es —A. Polygonum be llardii:
abe ‘led (Heldreich 877). —B. Polygonum douglasii: tube in clusters er & Porter 9722). — Polygonum
A ener a tubercles with = {з= we De Craene 975). T Polygonum cori um: smooth to pitte 4 surface with
striae (Jepson s.n.). —E. Polygonum tenue: pitted surface (Puissant s
ret Кл surface (Porter & Po ter 7555). =G

— Е. Polygonum polyg valoides subsp. kelloggit:
з. Polygonum tiie (Foure ade 5962): smooth with pits. —H. Poly-
gonella fimbriata: detail of granular rib d 6825). —l. Polygonella articulata: pitted surface with striae (Bodin
s.n.). Bars = 10 um, except A and | = 100

Annals of the
Missouri Botanical Garden

! j pm
Figure 9. LM micrographs of transverse Bug e tions of pericarps of Polygonum and Polygonella. —A -
hgonum ! der iaa (Puissant s.n. Bar m. —B. Polygonum oxyspermum subsp. гай. (Corbiére 5306),
TS. Bar = 70 wm. —C. Polygonum bellardii (He “dre ch 877 ), TS. Bar = 30 pm. —D. Polygonum shastense (Carpenter
s.n " 15, Ваг = 20 om — E, Polygonella polygama (Curtiss s. n.), LS. Bar = 15 um. —F. el aban molliaeforme
schy 778), LS. Ba 10 um. —G. Polygor en afromontanum (Hedberg 377), TS. 12 = ye 1. —H. Polygonella
. Polygonum tenue (Greene s.n.), LS. Bar = 20

americana (Fischer 10), TS. Bar = 20 pm

Volume 91, Number 2
2004

Ronse De Craene et al.
Taxonomic Status of Polygonella

335

mum subsp. гай: Fig. 9B). More or less similar wall
structures were observed in species of section Du-
ravia (e.g., Polygonum douglasii, Polygonum tenue:
Fig. 91), section Tephis (although the convolution is
more important and it lacks the dendritical branch-
ing: Fig. 96), and only rarely in Polygonella (e. g.,
Polygonella americana: Fig. 9H). Almost straight
radial walls (< 40 jm wide) with narrow lumina
occur in other species of section Duravia (e.g.. Po-
lygonum coarctatum, Polygonum shastense, Polyg-
( Fig. 9D), most Polygonella
Polygonella articulata, Polygonella polyga-
ma: Fig. OE), and in section Pseudomollia (Fig. OF).
Here the lumen appears narrowly rectangular, x-
shaped to triangular with the broad base on the
inner tangential wall. Dendritical canals are not ob-
served.

onum californicum:

aim.

e.g.,

poem

As emphasized elsewhere (Ronse De Cra-
ene et al., 2000), there is no link between the shape
of the exocarp cells and the outer surface of the
fruit
CLADISTIC ANALYSIS

The cladistic analysis resulted in 108 trees of
179 (consistency index (CI) 0.402, retention
(RI) 0.640).

Figure 10 and the 50% majority-rule consensus

length
index The consensus tree is shown in
tree with bootstrap and jackknife values in Figure
11. As is evident from Figures 10 and 11, the trees
obtained are relatively well supported (given that
all characters used were morphological). Two major
clades can be recognized, one containing all spe-
cies of section Duravia and the genus Polygonella
with a bootstrap-jackknife support of 67%/70%
and another weakly supported clade (BS 64/59%
containing sections Polygonum and Tephis. In pre-

— e

liminary analyses Polygonum molliaeforme consis-
tently fell within section Duravia, probably because
of convergences in morphological characters, and
was consecutively removed from the analysis. The
greatest internal support is for the group of species
recognized as Polygonum polygaloides and allied
species (cf. Hickman, 1984, BS 92%). Two clades
remain strongly supported within the Polygonum
clade (sect. Tephis) and a clade of three species
(Polygonum arenastrum, Polygonum | maritimum,
Polygonum oxyspermum). The 50% majority-rule
consensus tree shows the collapse of internal
branches in both clades. Species of Polygonella
form three paraphyletic clades with species of Po-
lygonum sect. Duravia, although two of the clades
are well supported. Synapomorphies can be recog-
nized for both clades, such as the presence of spi-

nules and ochrea morphology in the Polygonum

clade, and the Duravia-type of pollen and P/E in-
dex (except for one species) in the Duravia clade.

DISCUSSION

We found little unambiguous evidence to support
a full segregation of the genus Polygonella, because
several features known to be distinctive of the taxon
appear regularly in Polygonum, especially in sec-
tion Duravia. If the genus Polygonella is consid-
ered as sufficiently distinct, a number of species
from Polygonum sect. Duravia would have to be
transferred to Polygonella. This would considerably
reduce the number of characters necessary to dis-
tinguish Polygonella as a genus, unless other evi-
dence is found. Typical Polygonella species show
the following features: a single flower per node aris-
ing from the axil of a short scaly bract, a tendency
for unisexuality in some species, flowers often pen-
dulous with the abscission zone in the middle of
perianth mostly unequal with shorter
often reflexed outer tepals, and inner tepal lobes

the pedicel,

mostly larger, accrescent, and not appressed to the
fruit. Тера venation is reduced to a single mid-

vein. The number of stamens is usually not

duced, and the inner filaments are abruptly wid-

re-

ened. The pollen has a well-marked dimorphism of
the ektexine. Fruits are slender-stipitate and are
often beaked; the surface is smooth, mostly with
narrow lumen
without dendritical branching and straight radial
walls. However, as shown in Table 2

striae, and pericarp cells have a

and Appendix
4, the differences between Polygonella and the oth-
er tribes are not straightforward.
general characteristics

There are a few
for the species of Polygo-
17 although these are not shared by all, except

r the searious bracts, internodal branches, and
re pedicel abscission zone. The cladistic analysis
based on morphological characters does not permit
the identification of a well supported Polygonella
clade with these characters (Figs. 10, II). There-
fore, we cannot ascertain that these are synapo-
morphie

Vautier } (1949) and Horton (1963) interpreted the
presence of a single unbranched vein as a reductive
feature. Flowers of Polygonella (with tepals having
an average length of 3 mm, even becoming accres-
cent in fruit) are not necessarily smaller than those
of Polygonum s. str. It can be speculated that the
reduction in tepal vein may be an adaptation to an
arid environment necessitating less water transport.
Some Polygonum growing in similar dry habitats
also have a single unbranched vein (e.g.. Polygo-
num molliaeforme: Fig. 1E).

The exine of pollen of section Duravia and Po-

336

Annals of the

Missouri Botanical Garden

Strict consensus of 108 trees

Figure 10.

nr

г

manh

Strict consensus of 108 trees (length 179, CI 0.402, RI 0.640).

Fallopia cilinodis
Pol. aviculare

Pol. equisetiforme

Pol. arenastrum 2
Pol. maritimum 8
Pol. oxyspermum E
Pol. bellardii :
Pol. ramosissimum 1 ۾‎
Pol. undulatum S
Pol. afromontanum E
Pol. tenue |
Pol. douglasii

ssp. spergulariiforme @
Pol. bolanderi 3
Pol. californicum =
Pol. polygaloides

Pol. kelloggii

Pella parksii

Pella americana

Pella fimbriata a
Pella polygama 3
Pella gracilis е
Pella articulata T
Pol. minimum à
Pol. shastense a

Pol. = Polygonum; Pella = Polygonella.

Volume 91, Number 2 Ronse De Craene et al. 337
2004 Taxonomic Status of Polygonella

Jackknife 50% majority-rule consensus tree

Fallopia cilinodis

Pol. aviculare

Pol. equisetiforme

73 Pol. arenastrum

| =
64 Pol. maritimum
[

58

Pol. oxyspermum
Pol. bellardii

Pol. ramosissimum

Ж Ж анн Pol. undulatum
Pol. afromontanum

59

75
Pol. tenue
Pol. minimum
Pol. douglasii
ssp. spergulariiforme
Pol. shastense
92

peces Pol. bolanderi

67 | 68 93 ا‎ Pol. californicum
Pol. polygaloides
7 64 |
Pol. kelloggii
68 —— Pella parksii
| Pella americana
=e Pella fimbriata
78
— — Pella polygama
61 L—— — Pella gracilis

Pella articulata

Figure 11. Bootstrap and jackknife 50% majority-rule consensus tree. Bootstrap values shown above branches,
jackknife values below. Pol. = Polygonum; Pella = Polygonella.

Annals of the
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lygonella appears to have a mixture of the pattern
in Persicaria (an alveolate reticulum) and section
Polygonum (a finely granular surface surrounding

Skvarla, 1977; Hong & Oh, unpublished). Hedberg
(1946) argued that the similarities in pollen of Po-
lygonella and section Duravia are the result of con-
vergent evolution, because of differences in habit,
a disjunct geographical distribution, and the repe-
tition of the transition between the Duravia-type
and Avicularia-type within the Polygonella group.
Pollen of section Polygonum is invariably smooth
with scattered microspinules, and there is little or
no variation in this pattern. The Avicularia-type of
pollen can be readily recognized and differs from
the reticulate pollen found in some species of sec-
tion Duravia and Polygonella, a fact not recognized
by Hedberg. There are strong indications that the
similarity in pollen morphology of section Duravia
and Polygonella reflects a synapomorphy for both
taxa. Regarding the structure of the exine one has
a clear continuum of variation in the pollen of sec-
tion Duravia and Polygonella. On one extreme, the
pollen of Polygonella polygama and some Polygo-
num douglasii is reticulate-alveolate without di-
morphism (Fig. 31). A slight differentiation of the
size of the reticulate pattern between the mesocol-
pium/poles and ectoapertures is found in Polygo-
num tenue (Fig. 3F) and Polygonum douglasii (var.
latifolium; Fig. 3C).
nounced in pollen of Polygonum minimum (Figs.
3H, 4C), Polygonum douglasii subsp. spergulari-
forme, Polygonum shastense, Polygonella parksii,

This difference is more pro-

Polygonella articulata, and Polygonella fimbriata
with a reticulate-rugulate pattern. A change in the
pattern of sculpturing around the ectopores occurs
in Polygonum californicum by the presence of mi-
crospinules above the reticulation (Figs. 3B, 4B).

The area around the ectoapertures can also become
psilate to foveolate without traces of a reticulation
(Fig. 3E).

However, no clear link can be made between the
smooth exine with microspinules of Polygonum sect.
Polygonum (Fig. 3A), and the reticulate-alveolate
pattern of Polygonella and Polygonum sect. Duravia
(Fig. ЗВ, C, E, F. H. D.

recognition of section Duravia separate from section

This distinction supports the
Polygonum. The pollen differences between Poly-
gonella and section Duravia are almost inexistent,
and the two are clearly interrelated.

Interestingly, the pollen of Polygonum molliae-
forme of section Pseudomollia appears as interme-
diate between the Avicularia- and the Duravia-type
(Hong & Oh, unpublished).

graphical distribution of section Pseudomollia

Given the disjunct geo-

n

Iran and section Duravia in North America, it is
probable that a dimorphic exine has arisen inde-
pendently and more than once. Moreover, some
species of Fallopia, another genus of tribe Poly-
goneae (e.g., F convolvulus, Е scandens, F. dume-
torum: Ronse De Craene, unpublished), also show
a dimorphic exine (viz. a smooth mesocolpium but
punctate in the region of the colpi), as rightly point-
ed out by Nowicke and Skvarla (1977). Indeed, we
found that two pollen types occur side by side be-
tween different species of Fallopia (Hong et al.,
unpublished), viz. with a dimorphic exine or a more
uniform one.

By observing fruit surface patterns with the SEM
we could distinguish three main types: (1) smooth,
possibly with small pits; (2) with globular protuber-
ances (tubercles), lined along the anticlinal walls of
the cells, or aggregate in rows; (3) with intercon-
nected ridges separated by depressions (reticulate).
In addition, longitudinal striae may be present and
may be weakly or strongly developed. Wolf and
McNeill (1986) recognized four surface patterns for
species of section Polygonum occurring in Canada:
smooth, roughened, papillose, and striate-papillose.
A distinction. between smooth and roughened
achenes appears to be related to the collapse of the
anticlinal cell walls. The papillose and striate-papil-
lose types correspond with the types we described
as tubercled. The value of surface patterns appears
to be mostly restricted to the specific level in section
Polygonum, with the occasional presence of smooth
achenes and achenes having tubercles (e.g., Polyg-
onum arenastrum, Polygonum douglasii, Polygonum
tenue, Polygonum ramosissimum

hile we found highly dist saliv surface pat-
terns in some species, the different sections could
not be delimited solely on the basis of the fruit
surface, as different types overlap between the sec-
tions. There is also an intergradation between dif-
ferent patterns, with a smooth surface at one ex-
treme, and the highly distinctive tubercled surface
at the other. Stages in between are a rough surface
with shallow to deep pits, and with widely spaced
to aggregated tubercles.

iere is strong overlap between some species of
section Duravia and section Polygonum on the one
hand, and between section Duravia and Polygonel-
la on the other. Similar smooth fruit surfaces (pos-
sibly with pits lining the anticlinal cell walls) are
found in Polygonum sect. Duravia (e.g., Polygonum
Polygonum minimum) and section
Polygonum maritimum). The

californicum,
Polygonum (e.g.,
slender stipitate fruits of typical species of Poly-
gonella with smooth-striate surface (Fig. 7D, F) can
be often recognized in species of section Duravia

Volume 91, Number 2
2004

Ronse De Craene et al. 339

Taxonomic Status of Polygonella

(Fig. 7B, C). In contrast, other species of section
Duravia have a pattern more similar to Polygonum
sect. Polygonum (Polygonum douglasii: Fig. 8B,
The reticulate pattern

Cy
—

Polygonum tenue: Fig.
of Polygonum polygaloides and allies (Fig. 8F) ap-
pears as a completely divergent type, possibly de-
rived from a pitted surface as in Polygonum tenue.
Smooth and tubercled surfaces can occur side by
side in closely related species, or even within the
same species. Polygonella fimbriata has its fruit
partly covered with tubercles (Fig. 8H)

Sections of exocarps revealed two main patterns,
which were not necessarily linked with the external
fruit surface: (1) broadly square to cylindrical cells
(> 50 wm) with strongly convolute radial walls,
broad lumen and dendritical branching toward the
periphery; (2) narrowly rectangular cells (< 40 рт)
with straight radial walls, narrow lumen, and ab-
sence of dendritical branching.

The internal fruit wall in Polygonum sect. Pseu-
domollia resembles that of Polygonella to a great
extent in lacking dendritical canals, and with
straight radial walls and narrow lumen (Fig. 9F).
This pattern also occurs in species of section Du-
ravia centered around Polygonum californicum.

The presence of strongly convolute radial walls
correlates with a tubercled surface (rarely smooth)
and an absence of striae. All studied species of
sections Polygonum (Fig. -C) and Tephis (Fig.
ОС) show this characteristic pattern, as well as
some species of section Duravia (Polygonum doug-
lasii, Polygonum tenue: Fig. 91). Polygonella amer-
icana is an obvious exception for the genus with its
convolute radial walls (Fig. 9H).

CAN POLYGONELLA BE MAINTAINED AS A GENUS
SEPARATE FROM POLYGONUM?

Polygonum s.l. has always been difficult from a
taxonomic point of view, and several attempts have
been made in the past to improve the infrageneric
limits (see Ronse De Craene & Akeroyd, 1988, for
an overview). In contrast, Polygonella has always
been considered as distinct, first close to Atraphax-
is, then in the vicinity of Polygonum s. str. (Table

1). This study, however, has demonstrated that Po-
lygonum s. str. and Polygonella share several char-
acters that were thought to be distinctive, and that
a strict taxonomic separation at the generic level is
not tenable.

Based on the nom study the following conclu-
sions are signi t:

(1) Strict еб боз between Polygonella and
Polygonum s. str. is not supported. Characters of
several species of Polygonum sect. Duravia overlap

with those of Polygonella. Polygonum sect. Duravia
appears paraphyletic relative to Polygonella, with
a basal position for the polymorphic Polygonum
douglasii.

Especially on the basis of pollen (the distinctive
Duravia-type of pollen and the reticulate exine), as
well as fruit anatomy (rectangular cells with straight
radial walls and more or less triangular lumen), a
separation of section Duravia from section Polyg-
onum, and including Polygonella, is best main-
tained. Polymorphic species, such as Polygonum
douglasii, can have different characters spread over
different populations. For example, Howell s.n. (ex
Wibbe 7841), Carpenter s.n., and Porter & Porter
9722 have a tubercled fruit surface and a thick
pericarp; Howell s.n. (ex Wibbe 7842) has a
surface with a thin pericarp. Similarly, pollen of

smooth

Polygonum douglasii subsp. spergulariiforme
strongly resembles the Duravia-type, while the oth-
er samples of Polygonum douglasii studied are in-
termediate with little differentiation between me-
socolpium and colpi regions. However, more
research in these polymorphic groups is clearly
needed. Also, the sampling for this study is too
limited to draw definite conclusions about the in-
terspecific relationships of section Duravia.

(2) Polygonum sect. Tephis cannot be well sep-
arated from section Polygonum. Both sections share
similar pollen morphology, fruit surface patterns,
and fruit anatomy. Distinctive features are the af-
romontane distribution and dimerous flowers of sec-
tion Tephis.

The pollen with rough exine with microspinules
and the roughly pitted fruit surface of Polygonum
afromontanum (Figs. 3G, 4A, 6D) is found in sev-
eral species of section Polygonum. Similarities with
Polygonum undulatum are even greater. Ronse De
988), however, maintained
mainly because of dimerous flowers

Craene and A
the section,
with keeled outer tepals, and the development of
two lateral veins on the tepals. Stamen number is
also six in Polygonum afromontanum (with 5 te-
pals) and Polygonum undulatum (with 4 tepals),
the two outer not being “duplicated,” as in Polyg-
onum molliaeforme (numbers may vary between 6
and 8). In Polygonum undulatum, the perianth is
dimerous, apparently by the loss of an outer tepal
The dilated inner filaments and
tepal epidermis (Hong et al., 1998) match those of
section Polygonum. However, the inclusion of an-

with two stamens.

atomical characters may support а subsectional
rank. Given the limited geographical distribution,
this could also be justifiec

(3) Polygonum sect. Pseudomollia is distinctive in
external fruit characters (winged lenticular achenes).

Annals of the
Missouri Botanical Garden

but shows overlap in characters of pollen and fruit
anatomy with Polygonella. These are probably the
result of convergences. The different phytogeography
(the former occurs in Persia, while the latter is re-
stricted to North America) supports this.

Section Pseudomollia Boiss. was originally erect-
ed on the basis of the lenticular achene with two-
parted style, solitary flowers, and overlapping
ochreae. Material investigated by Ronse De Craene
and Akeroyd (1988) had only five stamens, as the
outer were not "duplicated"; another specimen
missed one outer pair altogether. Haraldson (1978)
mentioned the presence of five stamens and two or
three staminodes; these probably represent the out-
er stamens. Rechinger and Schiman-Czeika (1968)
mentioned 5 to 8 stamens and suggested that an-
thers drop off easily, which might give the false
impression of staminodes. The reduction of outer
stamens and the inflated filament bases, coupled
with one unbranched vein per tepal, as well as the
1998) fit within
section Polygonum. Haraldson (1978) did not find

tepal epidermal cells (Hong et al.,

the anatomical differences important enough to
merit sectional rank. However, the fruit morphology
(Fig. 6C) with lateral winglets along the beak is
quite distinctive, as well as the pitted reticulate
fruit surface. Also, the pollen with dimorphic exine
and distinctive sculpturing is not matched in sec-
tion Polygonum. The absence of secondary ramifi-
cations of the tepal veins is another distinctive fea-
ture, also found in Polygonella and some species
of section Duravia. Given the extended proposal in
this paper for delimiting the genus Polygonum s.
str., Pseudomollia is best maintained as a section
of Polygonum.
SECTIONAL AND SUBSECTIONAL DELIMITATION
Polygonella appears nested within a well-defined
genus Polygonum. Characters shared by species of
Polygonum have been listed in Ronse De Craene
and Akeroyd (1988) and include the dilated inner
filaments with occasional replacement of the outer
stamen pair by single stamens, or their reduction,
the absence of structural nectaries, similar tepal
epidermal cells, the single vein per tepal, and the
difference between outer and inner tepals. To re-
Весі more natural monophyletic groupings, the
merging of Polygonella within Polygonum is indi-
cated and given below. Alternatively, the genus Po-
lygonella could be maintained and expanded as to
include all species of section Duravia. However,
this shift is not advisable, as one cannot find suf-
ficient diagnostic evidence to identify Polygonella
as distinct from Polygonum, besides the pollen. In-

deed, the maintenance of a generic status is exag-
gerated, compared to other genera such as Fallopia,
Persicaria, and Fagopyrum. For example, the in-
clusion of the genus Reynoutria Houtt. as a section
of Fallopia by Ronse De Craene and Akeroyd
(1988) has been supported by cytological studies
(e.g., Bailey & Stace, 1992). A similar logic is ap-
plied here for Polygonella. Polygonella may be
viewed as an extreme evolutionary line within sec-
tion Duravia.

Hickman (1984) proposed the rank of subgenus
Duravia for the North American species of Polyg-
onum (see introduction). We do not support this
subdivision on the basis of a range of characters
(the variation of Polygonum polygaloides falls with-
in Polygonella). Two distinctive features character-
ize Polygonella: the abscission zone is situated in
the middle of the pedicel, and the branches appear
internodal by fusion with the main stem. Polygo-
nella is best included within section Duravia of Po-
lygonum s. str. The characters shared by this sec-
tion are obvious: Duravia-type pollen (with all
possible intermediates), a reduced number of flow-
ers per inflorescence, a smooth fruit surface with
narrow pericarp of rectangular cells (P. polygaloides
has a distinctive outer surface), and a tendency for
the outer tepals to become strongly dimorphic from
the inner, with a single unsplit vein. A subdivision
of a subsection Thysanella separate from Polygo-
nella (as was done by Horton, 1963) appears su-
perfluous as the differences enumerated for Thy-
sanella are made irrelevant by the inclusion of
species from section Duravia within Polygonella.

We propose the following sectional division for
Polygonum sensu stricto:

Polygonum L. sect. Polygonum

Subsection Pelygonum (L.) Ronse De Craene &
`.-Р. Hong, stat. nov. TYPE: Polygonum av-
iculare L.
Subsection Tephis (Adans.) Ronse De Craene &
5.-P. Hong, stat. nov. TYPI
dulatum (L.) Bergius =

©: Polygonum un-
Atraphaxis undu-
latum L.

Polygonum sect. Pseudomollia Boiss. TYPE:

Polygonum n orme Boiss.

avia S. Watson

Subsection 3 (S. Watson) Ronse De Cra—
ene & S.-P. Hong, stat. nov. TYPE: Polyg-
onum californicum S. Watson

Subsection Polygonella (Michx.) Ronse Decra-
ene. & S.-P. Hong, stat. nov. TYPE: Polyg-

onum articulatum L.

Polygonum sect.

Volume 91, Number 2
2

Ronse De Craene et al.
Taxonomic Status of Polygonella

341

A key to the sections and subsections is pre-
sented in Appendix 2.

We have shown that the notion of Polygonella as
an independent genus should be abandoned. The
results of this study reflect the need for a renewed
investigation of the North American species of Po-
lygonum. With a few exceptions no substantial mo-
lecular studies have been performed in the Poly-
gonaceae, especially in the genus Polygonum. This
would be a helpful addition to our morphological
investigations. The understanding of the internal
relationships of Polygonella to section Duravia
could be highly improved, as our study does not
clarify the internal relationship of the clade opti-
mally.

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1-50.

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Laubengayer, R. A. 19 Studies in the anatomy and
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Smets.

E f & D. J. Crawford. 1995. Pleistocene refu-
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1

Lewis,

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—— 1958. Eu

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Nesom, G. & V. M. Bates. 1 . Reevalutations of infra-
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^
V
^^
ее)
—

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—
-

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———. 19

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Torrey

Preliminary. notes on floral devia-

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е Amer. N
Webb, D. A. & 4 a Pp. 70—
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Valentine, S. M. Walters & D. A. Webb (editors), Flora

Europaea 1. Cambridge Univ. Press, Cambridge.

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Rhodora 40: 309—
Wolf, S. J. ¢ M Ne 1986. Synopsis and achene
morphology of Polygonum section Polygonum (Polygon-
aceae) in Canada. Rhodora 88: 457—479.

APPENDIX 1. Origin of species studied, with their
synonymy. I ies used in the cladistic analysis are
marked with *

e dee Lini secl. Polygonum

. Polygonum | ‘шаге L.*

SOUTH CA. Kimberley region: Kalkdrift,
Brueckner 771 0 PS). BELGIUM. Bruges, S9 1
pickled: Ronse De Craene 25 Lb (LN). 5 al
Prov.: Fuengiola, Nanfeldt 15203 (UPS) (pollen).

2. Polygonum achoreum Blake

U.S.A. Wyoming: Crook Co., Sundance, Porter & Por-
ter 8384 (UPS
3. Polygonum | maritimum L.*

FRANC ouches-du-Rhóne: Camargue, étan
d'Iland. Nordin 102 (U IPS). GREECE. Kos: W of Tin ae
ion, Davis 67953 (Е
4. Polygonum erectum

U.S.A. Illinois: e Bebb s.n. (UPS). Penn-
с Delaware Co., 1 mi. NE of Broomall, Wheeler

E Dou adn bellardii All.*
GREECE. Thessaliae: Pharsalum, Heldreich 877,
Herb. Bullemont 2369 (LV). HUNGARY: Herb. De Dieu-
2 5 (I
6. а ag 5 Sibth. & Sm.“
TUNISIA. r hotel Toumana, Ronse De Cra-
ene 975 ERA 309 Lt ) (LV)
. Polygonum енип Воге
U.K. Devon: Prawle Point, E.
ж (spirit 405 Le)
3. Polygonum oxyspermum Meyer & Ban ex Ledeb.
subsp. гай (Bab.) D. ы Webb & Chater *
FRANCE. Manche: Vauville et Denneville, L. Corbière
5306. ex Herb. a 843 (LV).
9. ia peni ramosissimum Michx
US

. Kansa . Mary's, P. A. Боны s.n. (LV).

u*
Prawle, Ronse De Craene

—
—
3

—

* Polygonum sect. Te
1. Polygonum e Gre е

KENYA. Nanyuki Distr.: Mt. Kenya, NW slope along
Sirimon, Hedberg 4320 (UPS). EE Kaffa Prov.:
Danish-Ethiopian Botanical Expedition 1972-1973 1622
(K). S Bale Prov.: Ririka, Hedberg 377 (UPS).
2. 5 undulatum (L.) Bergius*

SOUT CA. Humansdorp Distr.: 2.6 mi. from
Assegaai Bosc oh, Fourcade 5962 (BOL). chc in aper-
tis ia Schlechter 5974 (E).

e Polygonum sect. Pseudomollia
1. Polygonum molliaeforme Boiss.

Kuh-Daena, Kotschy 778 (UPS); Denawand,
r 8181 (К); Kuh-Daena, Kotschy s.n. (type) (E).

ө ооа sect. Dura
. Polygonum eg um 1 Meis
U.S.A. Се. P of Oroville, Heller
11763 (N Y); E кї г, Jepson s.n. ex Herb. Wibbe 92-
7830 (LV); Eal qiie viii 1892, don s.n. (UPS) (pollen);
Glen Co., 8 mi. E of Newville, A. A Heller 11553 (E).
2. r polygaloides Meia n.*
U.S )re

egon: Howell s.n. (LV); ex Herb. J. Wibbe,

Volume 91, Number 2
2004

Ronse De Craene et al. 343

Taxonomic Status of Polygonella

T. Howell s.n. (BR). Wyoming: Uinta Co., Snake River.

Nelson & Nelson 6463 3 (UPS). C pr ver Nez Percez Co.,
Lake Waha, . G. Heller 4 (E).
Subsp. kelloggii* D Gree ne) ss is | = Polygonum

kelloggii Greene]: oming: Johnson Co., Big
Horn Range, W of Buffalo, Circle Park, Porter & Porter

7555 (UPS).

Subsp. confertiflorum* (Nutt. ex Piper) " kman | = Po-
lygonum confertiflorun m эе ex Piper]: U.S.A. Califor-
nia: Modoc Co., 9 mi. X Camby, Bac salut & Smith
5982 (UPS). CANADA. Saskatchewan: Battle Creek,
Herb. Geological Survey 7 yos 12890 (E).

3. Polygonum shastense Brewer

5.A. California: E North Peak, Nygsen s.n. (UPS).
ornia? Placer Co., M. Carpenter s.n. ex Herb.

Wibbe 92- 1 (LV); N ane s above C oldsham, Sierra Ne-
vada, C. F Sonne s.n. ex Hed Wibbe 92-7879 (LV).

4. Polygonum tenue Mic B
US Massachusetts: is Blue Hills, Porters

1346 z PS): Baltic Co., P. A. Puissant s.n. (LV), Greene
s.n. pss North Carolina: Asha Co., bluff Mt., Leonard
А al, 2038 (Е).

5. Polygonum a aan К. Greene*
J.S.A. Placer Co. a Nevada Mts., A. М. Carpenter
T = 78 10 (LV). bd dap Southern
А slope of Sierra Madre, Porter & Porter
9722 (UPS). ы base of Stein’s mountain, Howell
s.n., ex Herb. Wibbe 92-7841 (LN).

Jregon: Siskiyou
Mountains, Howell s.n., ex He rb. Wibbe 92-7642 (LV).
As P. douglasii greene var. montanum Small: U.S.A. Mon-
tana: prar 5 Rydberg & Bessey 5364 (K). Nevada: Wash-
ol Co . Rose, Nevada o nod Experiment Station
tid C. L. Brown s.n. (E
Subsp. onda (Meisn. ex Small) өш, kman | =
Polygonum coarctatum die uh ex Meisn.]: U.S.
Oregon: Grants Pass, Hou x Heb. Ье 92-
7881 (LV). Lyal 1858 (К), bis. 1210 (UPS). Califor-
nia: University of California Jepson Herb. (lectotype of P.
а (E) ا‎ Co., Hettenshaw Valley, 5. K. Har-
Trinity Co., Van Duren n 3 mi.

below Hetten: ee valley, S. K. Harris et al. s.r
6. LN paneer rele ex A. Gray

U.S. di a Hills, C. G. Pringle S. N., ех
DE Wibbe 92 7820

7. Polygonum er C ham. & Schlec

U.S.A. California: San Francisco, Golden Gate
A um Rose 47103 (UPS).

8. Polygonum minimum S. Watson*

J.S.A. Washington: : ascades, Stevens Pass, Sandberg
& Rikers 799 (BR, UPS). Montana: on trail to Sperry
Glacier, L. M. Umbach 823 (E).

* Polygonella

1. Polygonella americana (Fisch. & Mey.) Small*

U.S.A. Texas: Cat. Springs, Fischer 10 (UPS). Arkan-
sas: Hot Springs Co., Malver гп, Palmer 8473 (К). Ala-
bama: Blount Co., Black waren Creek, Meisner 1845
(BR).

2. prat risas (L.) Meisr
U.S.A. Massa Ps etts: Oakes? s s.n. c New Jer-

sey: W 9 ury, Henry S. Conard s.n. (LV); Middlesex Co.,

South Amboy, s s.n. (UPS).

3. Polygonella re (Vent.) Engelm. & Gray [ = Po-
lygonella وا‎ ichx. |*
U.S.A. North Caro lina: Brunswick Co., Orton Plan-

tation Buen, Godfrey 1046 (K). California: Curtiss s.n.

(UPS). Florida: Indian River, Curtiss 2433 (LV), Curtiss

5525 (К); Palm Beach, artin 5525 (E).

4. учит parksii Cory*
U.S.A. Texas: Leon ne

sort, Codi & Correll 3

5. Polygonella SM (Elliott) Horton*
U.S.A. Florida: Tampa, Blanton 6825 (S).

6. Polygonella gracilis Meisn.
U.S.A. Mississippi: Sandy barrens, Pass Christian, А.

B. Langlois 177, ex | 92-7817 (1 z Florida:

Orange Co., Killarney, O. Ve stulund s.n. (UPS

Normangle, Hilltop lakes re-
K).

un

APPENDIX 2. Key to (sub)sections of Polygonum sensu
stricto.

la. Flowers dimerous, fruits usually lenticular.
2a. Small annual herbs, pollen dimorphic, fruit
surface tubercled with Аша, wings --------
y "udomollia
2b. Small to large ade bulla monomorphic
(Avicularia-ty pe). fruit surface smooth to pit-
ted subsect. Tephis
b. Flowe rs pentamerous, fruits usually trigonous.
За. Flov in clusters of 2 to 4(6) per

=

vers borne

tepal vasculature dendritical
subsect. cu

3b. Flowers borne singly « on each node (rarely
or more), always with 8 stamens and dn
carpels, pollen окота type or derived
within, tepal vase ee dendritical or re-

duced to a single

la. Bracts su сч individual flowers ог
flower leaf-like with papery
ochreolae, abscission zone when present

icularia-Aype,

clusters

just below flower
subsect. Duravia

. Bracts sulla бй individual flower

-—
~

scarious, abscission zone in the middle
of the pedice
8 subsect. Polygonella

APPENDIX 3. db ic a E in the cladistic analysis
„ 1857:

897:
Webb & Chater, 1964; Wheeler, 1938;

Wo lf & E; ES 1986)
l. Habit: erect to ascending herbs, rarely shrubs (0).
prostrate to creeping herbs (1), climbing herbs (2).
2. Leaf аре ovate ане (О), ovate to lanceolate (1),
:eolate-linear

3. Ochrea зне огне entire (0), two-cleft (1), lacerate
2).

4. Ochrea at maturity: entire (0), lacerate (1)

5. Leaf base: jointed with ochrea (0), not or obscurely
so (1).

6. Awns on top of ochrea: absent (0), present (1).

7. Heterophylly: absent (0), presen

8. Internodal fusion of branches: absent (О), present (1).

9. B od with numerous flowe ie (0). with 2
to 4(6) flowers/node (1), with 1(2) flowers/node (2).

10. Bracts of flowers: leaflike with pellucid ochreolae (0).

scarious (1), scarious with awns (2)

Annals of the
Missouri Botanical Garden

N
A

pn exserted from ochreola: not (0), barely so (1),
entirely

2. Pedic d orientation at fruiting: erect (0), curved (1).
3. Abscission zone of flower: absent

(0), against the base
of the flower (1), in the Е of the pedicel (2).
Gender distribution: bisexual (0), unisexual—gyno-
monoecious or dioecious (D.

5. Differentiation of outer and inner tepals at fruiting

(shape): subequal (0), slightly dimorphic (1), highly
dimorphic (2).

Jifferentiation of outer and inner tepals at fruiting
(size): subequal (О), outer smaller (1), inner smaller
2

. Division of perianth parts: below the middle (0). up
8 $e middle (1).
val venation: trifid (0), dendritical (1), only midvein

. Outer tepals at. maturity: flattened (0), angular-cuc-
culate (1), with a prominent keel (2

. Outer tepal orientation at fruiting: erect (0), reflexed
(

. Lateral walls of tepal epidermal cells: + straight (0).
Ta undulating (1).

. Cutic " ar striations оп (ера! epidermal cells: random
0), 1 OWS (1).

=

3. Ee number: eight (0), occ ccasionally less than eight

(1), always less than eight (2

. Stamen reductions: eight stamens present (0). outer
stamen pairs replaced by single stamen (1), outer sta-
men pairs partly incomplete (2), outer stamen pairs
with sterile anthers or lost (3), inner stamens missing

25. Filament shape of three inner stamens: not dilated or

only at the base (0), gradually dilated toward the base
(1), abruptly dilated in the middle

Trichomes at the base of the filaments: present (0),

absent (

. Pollen size 6 axis small to medium, <
(0), large, = 25 1).

. P/E ratio (pollen size): 1. 8 14 (0). 1.5-1.8 (1).
Apertural margins: absent (0), similar texture to the
rest of the grain (1), different texture from the rest of

the grain (2).

=

. Achene n proudly ovate (L <

О. Achene apex: wit en beak or with

. Ektexine differentiation: none (0), two distinct zones

. Mesocolpial ridges: not differentiated (0), strongly de-

veloped (1).

2. Pollen ektexine sculpturing pattern: smooth to rough

5 -punctate (0), foveolate to reticulate (1), bac-
culat

33. Pollen = mic Хал amg absent (О), smooth (1).
34. Pollen type sensu one

g (1946): Avicularia-type
(О), RM Eos (1), oth г (2).
andular rim aa gynoecium: absent
(О), pres it (1).

. Me D. “of flowers: trimerous (О), pentamerous (1),

dimerous (

: о id three (0), two (1).
. Occurrence of fruit dimorphism:
ith

absent (0), present
at hae same n M 1 a distinction бА зеп early-
апа late-season fru
5W) (0). inter-
mediate (1, = W) (1), lanc colt is 2W) (2)
ry short beak
(1

v

(0), with conspicuous to very long beak

‚ Stylar development: short and equal ir in size to

stigmatic lobes (0), two times as ei as stigmatic
lobes (1), ats stigmatic lobes (2
ase: not < itate or with very short stipe (0),

conspic iint d stipita te (1).

hene shape in transection: subangular (0), with two
convex and one co side (1).
Achene covering by pene included (О), shortly ex-
serted to 1/4 (1), stone exserted above 1/4 (

5. Primary sculpturing pattern: smooth to incons jicu-

ously pitted (0), with interrupted longitudinal ridges
with reticulate pattern

. Secondary sculpturing pattern: tubercules absent (0),
1).

present (

. Longitudinal striations on achene: absent (0), present

. Radial walls of pericarp in longitudinal section:

od (0), convolute (1).
ness о 8 0 arp in longitudinal section: < 40
peer )), > 40 1).

. Shape of lumen of pericarp cells: broadly rectangular

(О), narrowly rectangular (1).

‚ Presence of dendritical canals in pericarp walls: ab-

sent (0), present (1).

Volume 91, Number 2
2004

Ronse De Craene et al. 345

Taxonomic Status of Polygonella

file]

Appendix 4. Data matrix for cladistic analysis. Pol. = Polygonum; Pella = Polygonella. {Exported from MacClade

0 0 1 1 2 2 3 3 4 4 5
1 5 0 5) 0 5 0 5 0 5 0

Fallopia-cilinodis
Pol._aviculare
Pol.-equisetiforme
Pol._arenastrum

Pol._ramosissimum

Pol.-undulatum

Pol..afromontanum
l._tenue

Pol. minimum
Pol.-douglasii

Pol. “douglas subsp.

Pella-fimbriata

200000000121?200001000100000000010201000011000000111
11110010?000100001000011111000001001?200101011101111
111000001010101001000000110000001001?00010000101111
1111000020101000110000111100000010010200001?1?00001
111100001010100001000000110000001001000000?10000001
1111000010201000010000001100000010010101?01207?00001
01110000102010000110100011000000100101010100?101111
01110010?201010100110102111000000100?020001?200101111
011?20000102000000?210012011100000100210?010011001111
01?210000?2020?20000020011?1110000110021010?2000000111?
0?010110?200010020100100011011012010101100000??11111
21000000102010020100101?110110120101001?10010000001
o?000100?202110000110100011001012010101100100??01111

02000100202010000110100011012112010101010100??01001
210000002021100101010100111110120101002011010010010
02011000200010120?2011001101211201010021??000000010
0201100020001012022010001111211?0101002120000010010
020000002000101202101112110110120101011121002000010
02000000200010120?10110011011012010101110000?000010
020001112120??2100200100021111012010100112000001????
0100000121?0210102010000210100020101001101010010000
0200000121?202021020100002111211?0101001110000011111
020000012121200202001000210110120111001100010010010
0100000121112101020010002101101201010011210?0000000
0200010122?02?20020000001111101201010021210?0101111

[Note that some polymorphic entries were converted to missing data, represented by ?]

POLLINATION BIOLOGY OF
ARISTOLOCHIA
GRANDIFLORA
(ARISTOLOCHIACEAE) IN
VERACRUZ, MEXICO!

К. S. Burgess,’ J. Singfield,?
V. Melendez,? and Р. G. Kevan’

ABSTRACT

and usn idden prote in-rich substrate

which become el

protogynous а ind subsequently release pollen, a varie

A
T

in the po. Howe ers on the first day of anthesis. Althou

r po lination and allow the pollinators to esc win on qe second day of ean On the first Be of anthes
ibus ‘rs’ strong carrion odor and color gradients draw pollinators toward the

The flowers of Aristoloc hia grandiflora are sapromyiophilous trap blossoms that deceive their visitors with optical
bs

most effective pollinators are large oe mostly Calli-

the flowers are
of floral changes occur that discourage fu ie insect visitation
sis the

ceptive gynoste mium deep within the

flower. Constricting floral tubes with trichomes oriented toward the poa aid in capturing and ipis the

insects. On the next day, the flowers change to male phase and pollen is deposited on the pollinator. Flowe

structure

and function n change to release the pollen-dusted pollinator. To aid in pollinator release, the floral odor disappears,

color cues

e lis this is not relevan

Key words: Arist

tolochia grandiflora, Aristoloc

ange, hairs relax, and the constricting areas of the tube are opened. Pollination appears to be a two- -day
process for any given flower with floral senescence by the third day. Flo

ral visitors do ne it in the flowers, but we

t to pollination. Comparisons are made with other Aristolochiacea
'hiaceae, brood site provision, Calliphoridae, Dias, insect interac-

tions, Phoridae, pollination biology, protogyny, sapromyiophily, Staphylinidae.

There are many examples of how plants deceive
their pollinators to ensure pollination events (Dafni,
; Proctor et al.,

—

296). In some of the more
elaborate examples, м plant benefits from such
interactions by securing the transport of its pollen,
whereas the pollinator does not benefit. This is es-
pecially true for the Orchidaceae (containing the
majority of species pollinated by deceit), as most
insects will not eat pollinaria (Faegri & van der
Pijl, 1979). However, in many examples of floral
deceit some reward, including false pollen (e.g..
Melastomataceae) and shelter (e.g., Araceae), are
provided. Brood site mimicry, especially by scents
and sometimes appearances of carrion, dung, and
fungi, is well known in fly pollination through sap-
romyophily (Vogel, 1990; Larson et al., 2001) (or
sapromyiophily of Proctor et al., 1996) and its
equivalent involving beetles, saprocantharophily
(Bernhardt, 2000). Although Faegri, and van der

Pijl (1979) combined the characteristics of both fly
and beetle pollination by such deceit under the
syndrome of sapromyiophily, characteristics of this
syndrome include: more or less radial floral parts
with depth; lantern-shaped floral parts with filiform
appendages; dull floral colors (dark brown/purple/
green) often checkered with dark spots; odor resem-
bling that of decaying protein; the presence of os-
mophores (scent glands); the absence of nectar
guides, nectar, or other primary resources (Faegri
& van der Pijl, 1979; Vogel, 1990; Proctor et al.,
1996). These features can be found in flowers of
Asclepiadaceae, Araceae, Orchidaceae, Aristolo-
chiaceae, Sterculiaceae, Rafflesiaceae, Hydnora-
ceae, Taccaceae, and Burmanniaceae. Sapromyi-
ophily can occur with or without some form of
imprisonment (trap or semi-trap blossoms) of the
insect by the flower (Proctor et al., 1996; Faegri &
van der Pijl, 1979).

e thank Robert Bye, Director of the эксн а UNAM, 588 re inares (UNAM), Carlos Vergara, Led

* p io try, Universidad de Las A
de Biología Tropical “
thank Pablo 1 Saide (FMVZ

7

Instituto de Biología.

a, México, and Delfin

ación

NAM. with the proje We also

) for help with insect identification, and lan Smith at ds Unive К Guelph

Imaging Facility, College of Biological Sciences, for help with the figures. Some funds were made available through a
. K.

grant from the
? Botany Departme nt, University of Guelph,

z
2
=
a
Р

ent of Environmental Biology.

—
—
— (D
=
2
E
— 5
ч
=

uoguely

ANN. Missouni Bor.

atural Sciences and Engineering Research Council of Cana da
Guelph, Ontario, Canada NI“
ы наш Autónoma de Yucatán, (

University of Guelph,

to P.
; 21. канай »guelph.c
. P. 97000, Apdo. Postal 4- 116. Itzimna,

Guelph, Ontario, Canada NIG 2Wl. pkevan@

GARD. 91: 346-356. 2004.

Volume 91, Number 2
2004

Burgess et al.
Pollination Biology of Aristolochia grandiflora

The Aristolochiaceae comprise six genera: Aris-
tolochia L., Asarum L., Saruma Oliv., Euglypha R.
Chodat & E. Hassl., Holostylis Rchb., and Thottea
Rottb. (Pfeifer, 1960; Gonzalez, 1994). All are pol-
linated by deceiving their pollinators (although
some species may self-pollinate; Burke, 1890;
Peteh, 1924; Hou, 1983), and some may or may not
trap their pollinator. For example, the genus Asa-
rum secures pollination by deceit but without im-
prisonment, as in А. caudatum Lindl., which at-
tracts mostly mycophilous Diptera. In this case the
flies, during oviposition within the flower, acquire
pollen, but the larvae perish (Vogel, 1978a, 1978b).
A genus that imprisons its pollinators is Aristolo-
chia, comprising most of the 450 species within the
family (Pfeifer, 1960, 1970; Gonzalez, 1994). Like
many trap and semi-trap blossoms, Aristolochia has
protogynous flowers. During the female phase floral
visitors, pollinators or otherwise, are trapped within
the flower to facilitate pollen deposition on the stig-
ma. After pollination, visitors remain trapped with-
in the flower until pollen is shed over them during
the male phase of anthesis. After pollen release,
the flower opens to allow pollinators to escape and
carry pollen to another flower in female phase
1996). Although the general mech-

anism of pollination in Aristolochiaceae is under-

(Proctor et al.,

stood from studies on various species such as A.
bracteolata Lam., A. clematitis L., A. littoralis D.
A. la-
cordifolia

A. fim-

A. macroura Gomes, A.

Parodi, A. pilosa Kunth, A. grandiflora Sw..
Willd., A. linderi A. Berger, A.
A. sipho E Hér., A. tricaudata Lem.,
& Schltdl.,
glaucescens Kunth, A. goldieana Hook. f., and A.
T Linden (Sprengel, 1793; Hildebrand, 1867,
370; Delpino, 1873; Müller, 1873, 1883; Cooke.
1892; Ule. 1898a, 1898b,
1900; Knuth, 1909; Kirchner,
1911; Cammerloher, 1923: Carr, 1924; Petch,
1924; Knoll, 1956; Brantjes, 1980; Faegri & van
der Pijl, 1979; Hou, 1983; Hilje, 1984; Hime &
Costa, 1985: Wolda € Sabrosky, 1986; Razzak et
al. 1992; Hall € Brown, 1993; Proctor et al..
1996). detailed studies on the pollination biology
are Hilje, 1984;
Hall & Brown, 1993), and there are few compara-
tive studies between species (Brantjes, 1980; Sakai.
2002b

One of the more complex examples of sapromyi-
ophily is found in Aristolochia grandiflora Swartz,
which produces one of the largest flowers of the
Neotropical flora, and the largest in the Aristolo-
chiaceae (ca. 35 em diam.) (Knuth, 1909: Gonzalez.
1994). There are only two studies that attempt to
explore the pollination biology of this species. Cam-

biata
Glaz.,
briata Cham.

. 1898d. 1899,

scarce (see Cammerloher, 1923;

merloher (1923) studied its floral mechanisms at

the Botanic Gardens in Bogor, Java, and Hilje
1984) worked mostly on the phenology of a natural
population in Costa Rica. Although Cammerloher
1923) studied cultivated plants outside the natural
Neotropical range of A. grandiflora, both authors
described the pollination system of A. grandiflora

as consistent with the syndrome of sapromyiophily

—

—

with long-term imprisonment of the pollinators.
However, these studies contrast in the type of pol-
linators and insect visitors observed in two dispa-
rate populations, namely those native to Java and
Costa Rica,

provides a detailed assessment of the insect inter-

respectively. Because neither study

actions and floral phenology of A. grandiflora, and

—

because there is only sparse information on A.
grandiflora in its native range, the results of further
detailed observations contribute greatly to our un-
derstanding of the pollination biology of this spe-
les.

^

The goal of our research is to describe the pol-
lination biology of Aristolochia grandiflora growing
in its native habitat from a garden in Los Tuxlas.
Veracruz, Mexico. In this study we address the fol-
lowing objectives:

1. Determination of the mechanisms of sapro-
myiophily for long-term imprisonment in A.

grandiflora.

2. Assessment of the diversity and visitation
rates of floral visitors to flowers of A. gran-
diflora.

3. Determination of whether flowers of A. gran-

diflora provide brood sites for flower visitors.

MATERIALS AND METHODS

This study took place 1 km from La Estación de
Biología Tropical de los Tuxtlas, in the lowland
coastal rain forest of Veracruz, southeastern Mexico
(28 Apr.-9 May 1997).
known to be native to the area and flowers through-
out the year (Ibarra Manríquez & Sinaca Colin,
1987; Hilje, 1984) a
woody liana among cultivated vegetation in an open
habitat. Fifteen separate flowers of A. grandiflora
were used to make observations on floral structure

Aristolochia grandiflora is

nd was found growing as a

and insect interactions.

In order to describe the mechanisms of sapro-
myiophily for long-term imprisonment (Objective
1), floral structures important to the pollination pro-
cess of this species were 5 on one-, two-,
and three-day-old flowers (N = These н
overall condition of the flower, iaie stage of the
gynostemium, color of various floral structures, and

the presence/absence of odor. Herbarium speci-

348

Annals of the
Missouri Botanical Garden

mens were made of floral dissections and deposited
at the Herbarium of the Universidad Nacional Au-
tónoma de México in Mexico City.

To address Objectives 2 and 3, insect interac-
tions were observed across all 15 flowers prior to,
during, and after anthesis. In order to observe in-
sect visitation, insects were counted visiting, enter-
ing, and leaving flowers on the first and second day
of anthesis. Eight flowers were covered with mesh
bags to capture all insect visitors to the flower.
Flowers were then cut after the first, second, and
third day of anthesis based on insect interactions
with the flowers (i.e., fly entry and release). Two
flowers were bagged prior to anthesis as controls.
For example, Day 1: Three flowers bagged and cut
for dissection after one day of fly entry (end of the
first day of anthesis); Day 2: Three flowers bagged
after one day of fly entry and cut for dissection at
the end of the second day of anthesis; Day 3: Two
flowers bagged after one day of fly entry and cut
for dissection at the end of the third day of anthesis.

Bagged flowers were then taken to the field sta-
tion at Los Tuxtlas for longitudinal dissection, ob-
servation, preservation, and photography. To count
and identify (1) the insects contained within the
flower and (2) the insects released from the flower
but trapped within the mesh bags, bagged flowers
were fumigated in sealed plastic bags with ethyl
acetate to kill all floral visitors. Upon floral dissec-
tion, all floral visitors trapped within the flowers or
bags were collected and preserved in 70% ethanol.
Insects were not examined microscopically for pol-
len, although visual observations were made.
sub-sample of each of the insect families was taken
to the Entomological Collection of the Autonomous
University of Yucatán in Mérida for identification.

OBSERVATIONS AND RESULTS

MECHANISMS OF SAPROMYIOPHILY FOR LONG-TERM
IMPRISONMENT

Aristolochia grandiflora flowering patterns at our
site are consistent with continual flowering systems
of tropical lianas whereby relatively few flowers per
plant are at anthesis at the same time (Hilje, 1984;
Proctor et al., 1996). As in our study plants, such
flowering patterns are indicative of limited self-pol-
lination by geitonogamy. Flowers of A. grandiflora
at our site also had functional and structural mech-
anisms consistent with those used to describe this
species in the literature (Cammerloher, 1923; Hilje,
1984; Pfeifer, 1966). The flower (Fig. 1) has a uni-
seriate perianth, which includes a long filiform ap-
pendix (ap); the main perianth or limb (li); the fau-
a) or opening of the flower; the entrance or

md

ces (

br

OV

gy

"
ut g

an

ap

Figure l. Morphological terminology of Aristolochia
grandiflora floral structures: annulus (an), appendix (ap),
bracteole (br), fauces (fa), gynostemium (gy), limb (li), ova-
ry (ov), syrinx (sy), tube (tu), utricle (ut). (Re-drawn from
Gonzalez, 199 4.)

annulus (an); a trichome-lined tube (tu) connected
to the syrinx (sy), which opens into the inner cham-
ber of the flower, the utricle (ut); male and female
organs are located at the top of the utricle collec-
tively called a gynostemium (gy); and the inferior
ovary (ov) is subtended by a bracteole (br). General
observations on floral odor revealed that A. gran-
diflora flowers one day prior to and during the first
day of anthesis had a strong carrion scent, which
disappeared by the second day.

Additional changes in overall floral form oc-
curred during anthesis. As seen in Figure 2, the
length measurements made between the utricle and
the tube increased as the flower switched from fe-

Volume 91, Number 2
2004

Burgess et al.
Pollination Biology of Aristolochia grandiflora

Figure 2.

anthesis. —A. The angle between oral structure

Relaxation of. Aristolochia grandiflora floral structure to allow for insect departure on the second day of
these floral 's increased to 60 degrees on the second day of anthesis. cu

The ps bieen he floral tube and utricle wall prior to pollination on the first day of anthesis is approximately 28

degre

male to male phase (an increase in angle from 28

to 60 degrees). Table 1 details changes in floral
form, structure, and color over the first three days
of anthesis. Observations are based on floral dis-

sections made on one-, two-, and three-day-old
flowers. The first day of anthesis, starting shortly
after dawn, showed vibrant coloration of all struc-
tural components as the female phase of the gy-
nostemium progressed. Most of the flowers struc-
tural components (annulus, tube, syrinx, and
utricle) had erect trichomes and all had iusi tis-
sue. As the gynostemium switched from female to
male phase on day 2 of anthesis, a general deteri-
oration of the structural components of the flower
initiated. As seen in Table 1, the tissue of both the
syrinx and the utricle started to degrade, and the
trichomes of all structures flattened. The limb also
began to deteriorate and fold in at this stage, and
discoloration of various structures started. By t
third day of anthesis, the limb completely folded
in, trichomes were mostly absent from all floral
structures, and the tissues of all structures had
started to decay and brown.

INSECT INTERACTIONS (VISITATION AND BROOD SITE
PROVISION)

General observations of floral visitors to five Aris-
tolochia grandiflora flowers revealed that on the

day prior to the opening of the limb on the first day
of anthesis, large (ca. 5 mm) Diptera (Calliphori-
dae) were observed congregating along the limb
edge and on the appendix. Shortly after dawn on
the first day of anthesis the carrion-like odor in-
creased in intensity. Insect visitation was observed
10:30 A.M.

mately 200 insects were observed to be entering

to peak between 9:30 anc Approxi-
each flower during peak visitation with activity
dwindling to 13 insects between 11:30 A.M. and 12:
00 noon. Even though visitation (the total number
of insects entering a flower) dropped dramatically
by noon, flowers remained open until the next day,
potentially receiving more visitors, although this
was not observed. A more detailed observation of
floral visitation on the first day of anthesis showed
that of those insects immediately identifiable to the
researchers in the field, Coleoptera (ca. 7 mm) and
small (ca. 2 mm) Diptera (Phoridae) were the pri-
mary visitors in the ea
(ca. 5 mm) Diptera (Calliphoridae, Sepsidae, Mus-
cidae, and Heleomyzidae) were only found to visit

rly morning, whereas large

mid-morning, although Phoridae visitation contin-
ued throughout (Fig. 3).

pon dissection of the flowers at the end of the
first day of anthesis the average number of insects
per flower was 454 (Table 2). Although most insects
were Diptera: Phoridae (269) (ca. 2 mm) and Co-

350 Annals of the
Missouri Botanical Garden
Table 1. Floral structures important to the pollination 2 ess of Aristolochia grandiflora measured on eight flowers
de s

at the end of the first, second, and third day of anthesis

of trichomes on the structure (+ = erect; —

= sod ges notes on structure color (B

‘ture, status

black; Br =

urements include overall status of the struc
= beige; BI =

brown; P = purple: W = white).
Floral structure Day 1 Day 2 Day 3
Limb
Status rigid and open folding on guidelines folded/decaying
Trichomes erect/flattened absent absent absent
‘olor checkered (P/W) checkered (P/W) r
Annulus
Status rigid soft decaying
Trichomes erect/flattened + =
Color P/BI P/W P/Br
Tube
atus rigid soft decaying
Trichomes erect/flattened + — =
Color P to W P to Br/W Br
Syrinx
Status rigid decay starting decaying
Trichomes erect/flattened + — —
Color W Br Br
Utricle
tatus rigid decay starting decaying
Trichomes erect/flattened + — —
Color spotted (W/ P) Br Br
Gynostemium
Stigma lobes
Status stigma receptive stigma not receptive decaying
Color 3 Br Br
Anther
Status anthers closed anthers dehisced decaying
Color 3 Br Br

leoptera: Staphylinidae (144) (ca. 7 mm), a number
of large (ca. 5 mm) Diptera were found within the
flowers, namely; Calliphoridae (13), Sepsidae (7),
Muscidae (16), and Heleomyzidae (4). No insects
were found in the mesh bags outside the flower at
the end of the first day of anthesis

On the second day after ка release of large
(ca. 5 mm) flies (Calliphoridae, Sepsidae. Muscidae,
and Heleomyzidae) by relaxed angle of the perianth
tube and flattening of trichomes (Fig. 2; Table 1)
occurred between 8:00 A.M. and 9:00 A.M. This was
followed by the release of smaller (ca. 2 mm) flies
(Phoridae). Large (ca. 5 mm) flies (Calliphoridae,
Sepsidae, Muscidae, and Heleomyzidae) were ob-
served to leave the flower with large clumps of pollen
on their back. Upon dissection of the flowers at the
end of the second day of anthesis most insect taxa
initially found. within the one-day-old flowers were

now inside the mesh bags but absent from the flower
interior. These included all adult Diptera (Calli-
phoridae (9), Muscidae (4), and Heleomyzidae (1),
and most notably the Phoridae (366)) (Table 2).
Probably most notable was the presence of large
numbers of Staphylinidae still within an average
flower (218) and the occurrence of approximately
1000 Phoridae larvae on the utricle wall.
Dissections of bagged flowers cut after the third
day of anthesis revealed that almost all the insects
that were in the flower at the second day of «тасак
were now only found outside the flower within the
mesh bags (Table 2). These included Phoridiae (29)
and the Staphylinidae (203). There was also a large
number of Phoridae larvae found within three-day-
old flowers (approximately 400), although numbers
decreased from two-day-old flowers by more than

50% (Table 2).

Volume 91, Number 2
2004

Burgess et al. 351
Pollination Biology of Aristolochia grandiflora

+
©
Y
e

E
— 90% -
2
| 5 80%
$ 70%

EJ Staphylinidae |
= 0, . beetles ||
9 60 % (ca.7mm)

2 50% NA Large

= Dipteran Flies
E 40% 5mm)
Е:
| 0 iB Small
| = 30% Dipteran Flies
| hs 20% (ca.2mm)

Ф 0

a 10%

0% T
SP کی کے‎ Oo کی‎ S р ле P

| Sampling period

Figure The average number of Dipteran flies (large and small) and Staphylinid beetles (Coleoptera) observed

entering five flowers of Aristolochia grandiflora during peak

as a percentage of total insect visitation for each census pe

DISCUSSION

POLLINATION AND MECHANISMS OF
SAPROMYIOPHILY FOR LONG-TERM IMPRISONMENT

Although self-pollination has been suggested for
some Aristolochia species (Burck, 1890, 1892a,
1892b, 1892c, 1894) our observations on A. gran-
diflora suggest that this is most unlikely. Our re-
sults indicate that pollination in A. grandiflora is
consistent with the syndrome of sapromyiophily in
odor, color, and floral structure (Table 1) and ap-
pears to be a two-day process. The protogynous
flowers last only three days, but are attractive to
pollinating insects (Diptera and Coleoptera) only on
the first day of anthesis, which is when they are
most odoriferous and in the pistillate phase, al-
though a large number of insects are attracted by
odor to the general vicinity of even the pre-anthesal
flower. After pollination on the first day, anthers
release pollen onto insects trapped within the utri-
cle. On the second day of anthesis, pollen-laden
insects escape after the flower goes through various
changes in form and loses its scent. Mimetic color
and floral structures appear to entice visitors into
the depth of the perianth once odor has brought
them to congregate in the general area (Faegri &

visitation on the first day of anthesis. Means are expressed
riod.

1979; Dafni, 1984).
(Fig. 1), the large radial, funnel-shaped limb dis-

van der Pijl, Upon opening
played a blotchy pattern of purple and white with
blotchy purple guide-lines leading to the dark cen-
tral cavity of the tube entrance or annulus (see
Cammerloher, 1923; Hilje, 1984). Once the insect

visitors have proceeded past the annulus, our ob-

jai

servations from floral dissection suggest that insects

are directed to the utricle (site of pollination)
through a combination of floral structure (shape of
tube and trichome orientation) and color changes
(Table 1). The floral tube has grades in color from
a dark purple near the annulus to the brighter,
translucent utricle. Presumably, flies phototactical-
ly orient themselves to the light color of the utricle
as suggested by Hilje (1984)
(1923). Within the flower there
1) that act as filters for insect size selection (see
Hilje, 1984; Brantjes, 1980). Between the perianth
tube and the limb (annulus), and between the tube

and Cammerloher
are two sites (Fig.

and the utricle (syrinx) are constricted areas cov-
ered with stiff trichomes pointing in toward the utri-
cle that allow visitor movement in only one direc-
tion, as seems general for the genus (Knuth, 1909;
Cammerloher, 1923; Hilje, 1984; Hall & Brown,
1993) (also see Table 1).

Missouri Botanical Garden

Annals of the

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Volume 91, Number 2
2004

Burgess et al. 353
Pollination Biology of Aristolochia grandiflora

The transition from pistillate to staminate phase

is indicated by changes in floral odor, color, and

structure (Table 1). The switch is reported to be
physiologically triggered by the direct deposition of
pollen onto the stigmatic surface of pistillate flow-
ers (Pfeifer, 1966). Although limited to two flowers,
our bagged controls to which insects had no access
and thus pollen cannot have been deposited on the
stigmas, showed changes as in open-pollinated
flowers. We noted that in the staminate phase the
overall structure of the flower appears to relax at
the beginning of the second day of anthesis (Table
1; Fig. 2). The tube is no longer appressed to the
utricle as the angle increases between these two
floral structures. Hilje (1984) also noted an in-
crease in the diameter of the restriction between
the utricle and the tube at this stage in Aristolochia
grandiflora (Fig. 1). Presumably this relaxation of
the flower allows escape of the entrapped insects.
now bearing newly deposited pollen loads from the
dehiscence of anthers as observed in this study on
the morning of the second day of anthesis. Contrib-
uting to the release of insects were changes in the
trichomes (Table 1) throughout the tube and utricle
that become either flattened or brittle, and lose uni-
directional orientation (also noted by Knuth, 1909:
Pfeifer, 1966) (Table 1). At the same time, probably
contributing to insect release is the darkening of
the utricle from translucent white of the first day of
anthesis to brown in the second, which would re-
duce phototactic orientation (Table 1).

By the

rapidly (Table 1). In general, floral senescence oc-

third day of anthesis the flower decays
curs and the calyx is either ие ог falls
(Knuth, 1909; Pfeifer, 1966). W

persistent calyxes on fruits present at our site, al-

le did not observe

though fallen flowers had withered and dried quick-
ly (within two days: casual observations) in the sun.

The suite of characters (morphological, odor, and
phenological) we describe occurs with sapromyi-
ophily and allows for precise timing of events as-
sociated with successful pollination. The process
depends on the long-term (ca. 1 day) imprisonment
of the insect visitors. The exact timing of entry and
exit of visitors to any Aristolochia species has not
hitherto, but
showed a peak entry of insects around 10:00 A.M.

been recorded our observations
on the first day of anthesis, and exiting around 8:

30 the next morning.
INSECT INTERACTIONS (FLORAL VISITATION AND
POTENTIAL POLLINATORS

According to Brantjes (1980) some Aristolochia

species are specialized to capture specific fly spe-

cies or sizes, whereas many others capture a wide
variety of organisms that may not be effective pol-
linators. Thus, the potential pollinators of any Aris-
tolochia species are selected by floral size (as sug-
1909) and the
nature of the trap mechanism. Therefore, by mea-

gested by the review in Knuth,

suring the visitors thorax height and the distance
between floral structures that act as filters, non-
pollinators may be distinguished from potential pol-
linators (Brantjes, 1980). Petch (1924) conducted
studies on the native small-flowered species 4.
indica L. and A. bracteata Retz in Sri Lanka and
found that both were visited by a single insect spe-

—

cies of Ceratopogon (Diptera: Ceratopogonidae
However, we demonstrated a wide range of Diptera,
Coleoptera, Homoptera, and Hymenoptera impris-
oned in the utricle of A. grandiflora (Table 2).
Our study agrees with previous studies on the
pollination biology of Aristolochia that Diptera, es-
pecially Phoridae, Muscidae, and Calliphoridae,
are the predominant pollinators (Table 2). Although
high numbers of Staphylinidae were present in our
flower dissections, there is no evidence for beetle
pollination in our study. Bernhardt (2000) would
interpret A. grandiflora as a generalist system in-
corporating both beetles and flies given that the
species belongs to a genus of basal angiosperms.
Because our study does not exceed the third day of
anthesis, it is plausible that beetles may yet emerge
with viable pollen from rotting flowers. However,
studies consistently report that pollen is carried on
the backs of Dipteran thoraces (Delpino, 1873;
Knuth, 1909; Hilje, 1984; Brantjes, 1980; Hall &
Brown, 1993), indicating that the flies walk on the
utricle wall and have pollen — from the gy-
9). We found
most fly visitors to A. grandiflora were small Phor-

nostemium (Correns, 1891; Knuth,

idae, but based on our visual observations large

Calliphoridae and Muscidae were the flies that car-
ried pollen (Table 2). Although Phoridae visitation
was high, we suggest that the Phoridae are not ef-
fective pollinators for this species. Hilje (1984) also
found that the most abundant visitors to А. gran-
diflora flowers were Phoridae, but noted that it was
unlikely they were the pollinators because they car-
ried relatively little pollen. He, too, indicated in-
stead larger flies of the families Otitidae and Mus-
cidae. In Java, Cammerloher (1923) indicated that
the pollinators of A. grandiflora were large Calli-
phoridae even though he found the principal visi-
tors to be smaller Anthomyidae. The specific dif-
ference between our results and the two previous
studies may reflect differences in geographic loca-
tion, time of year, the availability and diversity of
pollinators, or combinations thereof. Cammerloher

354

Annals of the
Missouri Botanical Garden

(1923) studies were conducted outside the native
habitat of A. grandiflora, and Hilje (1984) did not
document floral changes and phenology to the level
of detail that we provide.

INSECT INTERACTIONS (PROVISION OF REWARDS:
BROOD SITES, MATES, FOOD, PREY)

We found a large community of Phoridae larvae
living on the utricle wall of flowers of Aristolochia
grandiflora indicating oviposition by visiting in-
sects (Table 2). Little is known about provision of
brood sites within the Aristolochiaceae. Asarum
caudatum provides a site for oviposition, but larvae
die (Proctor et al., 1996).
Aristolochia, including those studying A. grandiflo-
ra, who found larvae of Phoridae, Muscidae, and

Some investigators of

Drosophilidae within the flowers have shown that
the utricle wall acts as a brood site (Hall & Brown,
1993; Hilje, 1984), but again without larval surviv-
al. Wolda and Sabrosky (1986) studied flies asso-
ciated with the flowers of A. pilosa in Panama and
found no evidence of oviposition. They also noted
that no males were ever reported inside the flowers.
Three studies of different Aristolochia species in
Panama have shown female-biased trapping (Wolda
& Sabrosky, 1986; Carr, 1924; Hime & Costa,
1985), but for A. littoralis in Florida, the bias is
mainly to males, presumably attracted by a female
sex pheromone mimic (Hall & Brown, 1993). For
A. grandiflora, insect visitors of both sexes have
been shown (Cammerloher, 1923; Hilje, 1984), in-
dicating that co-habitational sequestration may pro-
mote mating.

It has been suggested that some Aristolochia spe-
cies may provide food rewards to visitors (Knuth,
1909); these include nectar, e.g., A. clematitis, and
mucilaginous stigmatic exudates (Hilje, 1984; Wol-
da & Sabrosky, 1986) although nectaries were not
found in our study species. Whether or not there is
a benefit for the pollinator for its services to the
plant is incompletely known, and rewards may vary
from species to species of Aristolochia and polli-
nator. Within the utricle lives a diverse community
of Coleoptera, Diptera, and Hymenoptera that may
show interesting predator/prey interactions (Hilje,
1984) (Table 2). The flower attracts many predators
to the utricle, possibly in search of protein-rich lar-
vae (Hilje, 1984). The primary predators for both
Hilje (1984) and our study were Staphylinidae (Co-
leoptera). The fact that Staphylinidae did not es-
cape from A. grandiflora flowers until the third day
of anthesis (Table 2) suggests that they may obtain
some benefit, possibly prey, from remaining Phori-
dae larvae. A greater than 50% decrease in larval

counts within day 3 flowers as compared to that of
day 2 also suggests the possibility of predation by
Staphylinidae (Table 2). However, in A. grandiflora
Petch (1924) suggested that a toxic chemical stored
in the utricle wall protects developing maggots from
predation.

CONCLUSIONS

Aristolochia grandiflora is a short-lived flower (3
days) of a continual blooming tropical liana. Its
suite of characters, including form and color of the
perianth, odor (its production and cessation there-
of), floral movements (including trichomes and the
perianth as a whole) with aging, and definitive pro-
togyny, place the flower within the syndrome of sap-
romyiophilous trap blossoms (Faegri & van der Pijl,

9). We suggest that the most effective pollina-
tors are the large (ca. 5 mm) Diptera (Calliphoridae,
Muscidae, Sepsidae, Heleomyzidae). Although we
did not quantify our observations, they were seen
exiting our study flowers with visible dustings of
pollen on their bodies. The flowers also attract and
trap large numbers of small beetles (Staphylinidae)
and small Diptera (Phoridae); however, we cannot
assess the role of Phoridae and Staphylinidae as
pollinators. Although brood site provision can at-
tract pollinators to the flowers of some Aristolochia
species (Disney & Sakai, 2001; Sakai, 2002a,
2002b), we cannot conclude this from our study.
The large Diptera (Calliphoridae, Muscidae, Sep-
sidae) have larval developments that are typically
more than a week (Smith, 1986), and much longer
than the life of the flower, where the falling flowers
of A. grandiflora in our study were withered and
dried within two days. The small Diptera (Phoridae)
may be able to mature on rotting flowers provided
they remain moist for long enough (e.g., at least a
week (Disney, 1983, 1989)). The flowers do not ap-
pear to provide nectar and we did not determine if
the flies ingested pollen, but those families we
found are not noted for pollenivory, except for pos-
i 2001). Thus,

we do not invoke mutualism between the flies and

sibly some Muscidae (Larson et al.,

the flowers, but rather attraction by deceit (Dafni,
1984). Results from our floral dissections and ob-
servations indicate a reduction in Phoridae larvae
in the presence of large numbers of Staphylinidae
beetles. Based on our observations, it is possible
that the beetles found within A. grandiflora flowers

—

e.g., Staphylinidae) may be predatory and feed on
Dipteran eggs and larvae deposited in the flowers,
but this idea remains to be tested.

Volume 91, Number 2
2004

Burgess et a
Pollination Biology of Aristolochia grandiflora

355

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Biotropica 18: 295—296

EXPERIMENTAL EVIDENCE
OF POTENTIAL FOR
PERSISTENT SEED BANK
FORMATION AT A
SUBANTARCTIC ALPINE SITE
IN TIERRA DEL FUEGO,
CHILE!

Mary T. Kalin Arroyo, ? Lohengrin A.
Cavieres,?* and Ana María Humana?

ABSTRACT

Seed burial experiments were conducted for 15

alpine spec ies derived from 15
S. Ch

> genera and 12 plant кы from a

subantarctic location on Cerro Riñón, Tierra del Fuego, 54°S ile. Batches of seed buried at 5 ст depth at 550 m

elevation in February 1996 were ко after 335, 363, a and 755 « and their status and viability Мага.

Thirteen species (87%), опе таг Acaena magellanica, Anemone ‘multifida, Azorella lycopodioides, Bolax gum-
К

mifera, Calceolaria biflora, Caltha ALME Draba magellanica, Empetrum ru pisi
Oremomyrrhis hookeri (marginal). Pernettya pum
while two i necio анаи us, Berberis bu sola) only ae d evidence

Gunnera magellanica, Luzula alopecurus,
ес

igh and showed little tendency to diminish over

eds

the two- year experime ntal period, indicating optimal 3 for seed survival in the alpine soil. Fits of the куно T

each exhumation date to the
estimates of 1623 days in Draba magellanica, 2779
s in Oreomyrrhis hookeri, and 59.
the beanie tic alpine site are among the highest reported

rds:

E

) da s in 5 1
83 days in Pernettya pumila. Y

ential model gave maximum seed longevity
3026 days in Gunnera DOLAR

vities for some species at

negative expor

"stima ted seed longe
for alpine species to

бте:
Chile, persistent seed bank, seed burial experiments, seed viability, Tierra del Fuego, transient seed

Examination of soil cores for viable and/or ger-
minable seeds has revealed the existence of exten-
sive soil seed banks in arctic and alpine vegetation
at several Northern Hemisphere locations (e.g.. Mc-
& Vavrek, 1989, and references therein:
Ebersole, 1989; Hatt, 1991; Ingersoll & Wilson,
1993; Chambers. 1993, 1995; Diemer & Prock,
1993; Molau & Larsson, 2000). McGraw and Va-
vrek (1989) estimated that up to one half or more
of the species present in the standing vegetation in
alpine and arctic sites could be found in the seed

Graw

nk.

Although the study of soil cores has been useful
in ascertaining that sexual reproduction is a com-
mon feature in the cold and harsh alpine and arctic
habitats, few studies have been carried out in such
a way as to be able to distinguish clearly between
the transient and persistent components of the soil

seed bank (e.g., Roach, 1983: Ebersole, 1989; In-
gersoll & Wilson, 1993). The soil core method has
an additional disadvantage. Because soil cores con-
tain seeds produced over a number of vears, even
with careful sampling so as to exclude seeds cor-
responding to the present years seed rain, very lit-
tle can be said about the longevity of seeds beyond
one year. Longevity of seeds in the soil constitutes
the vital information required for understanding the
relevance of a persistent seed bank in the context
of life-history theory (Brown & Venable, 1986:
Rees. 1996), and for the successful restoration of
degraded areas in many alpine and arctic sites
(e.g.. Urbanska, 1997

An alternative approach is to experimentally
bury batches of seeds of known age in the soil,
retrieving and examining samples for viability and/
or germinability at a series of programmed future

' Research supported by CONICYT Grant No. 1950461

vanced Studies in Ecology and Research in Biodiversity. Fi

and Grant P99-103 F ICM supporting the Centre for Ad-
ieldwork in Tierra del Fuego was conducted on the private

property of Forestal Trillium Ltda., to whom we e xpress gratitude for logistic support. We are grateful to Manuel Arrovo

Kalin for collaboration with collecting and pre paring seeds and digging the
encias, Universidad de €

? Departamento de Biolc ogía, Facultad de
‘ Departamento i Botánica, Facultad e Ci iencias Nature
160C, Concepción.

ANN. MISSOURI Bor.

burial sites

zhile.
y Oceanográficas, U odi de Concepción, Casilla

iles

thile. leaviere@udec.cl. *Address for manuscript correspondence

GARD. 91: 357-365. 2004.

358

Annals of the
Missouri Botanical Garden

dates (Baskin & Baskin, 1998). This method has
been employed for single or small numbers of spe-
cies from several habitats (e.g., grassland: Pavone
& Reader, 1982; tropical: Lonsdale et al., 1988;
sand dunes: Zhang & Maun, 1994) including high
mountains (Guariguata & Azocar, 1988; Spence,
1990; Cavieres & Arroyo, 2001; Schwienbacher &
Erschbamer, 2001). Nevertheless, the mos of
these studies have been focused on single speci

For example, Guariguata and Azocar (1988) buried
seeds of the long-lived, dominant paramo species
Espeletia timotensis Cuatrec. (Asteraceae) in its nat-
ural habitat for a period of one year. Spence (1990)
performed a seed burial experiment of just over one
year's duration on Chionochloa macra Zotov (Gra-
mineae), dominant in the low alpine region in the
Craigieburn Range in New Zealand. Cavieres and
Arroyo (2001) performed a seed burial experiment
of 3 years’ duration with the perennial herb Pha-
celia secunda J. К. Gmel. at different elevations in
the Andes of central Chile. Only Schwienbacher
and Erschbamer (2001) have experimentally eval-
uated the persistence of seeds in the soil for nine
species in the Austrian Alps at 2400 m a.s.l. How-
ever, they evaluated the fraction of seeds that re-
main viable in the soil only after eight months’
burial, reporting that six species showed high per-
centages of seeds that remain ungerminated;

only three of those species was there certainty that
the remaining ungerminated seeds were viable.

In this paper, we report the results of seed burial
experiments of 2 years’ duration carried out at a
subantarctic alpine location in Tierra del Fuego
(54°S), Chile, in order to detect the potential for
persistent seed bank formation. Persistent seed
banks, by definition (Thompson et al., , аг
those in which a fraction of the seeds of a species

%

not only remain in the soil, but are also viable for
at least one year after production. First, we deter-
mine whether 15 alpine species individually exhib-
it potential to form a persistent seed bank. Second,
we attempt to fit mathematical functions to our seed
burial results in order to estimate the length of time
seeds of the species studied could potentially re-
main viable in the soil. Third, we assessed whether
the persistence of seeds in the soil is related with
other characteristics of the seed such as the size
and shape, as it has been pp in other ecosys-
tems (e.g., Thompson et al., 3)

MATERIALS AND METHODS
STUDY SITE

Work was conducted in the alpine belt immedi-
ately above the Nothofagus pumilio (Poepp. &

Endl.) Krasser tree line lying at 450—500 m ele-
vation, on Cerro Riñón (54°S), located in the Pa-
tagonian Andean complex on the edge of the forest-
steppe boundary in Tierra del Fuego (Fig. 1). As is
found on inland mountains throughout Tierra del
Fuego, the dominant species are cushion plants
(Bolax gummifera (Lam.) Spreng. (Apiaceae), Azo-
rella lycopodioides Gaud. (Apiaceae)) and the pros-
trate shrub Empetrum rubrum Vahl ex Willd. (Em-
petraceae), these being accompanied by many
caespitose and rosette perennial herbs and slender
grasses (Moore, 1983; Arroyo et al., 1996; Mark et
al., 2001). Flowering in the eastern mountains of
Tierra del Fuego occurs from close to snow melt in
early October through to early March. Although not
quantified, peak fruiting occurs in the interval of
February to early March.

Available climatic data for the general area of
Cerro Riñón are limited. Annual precipitation on
the forest-steppe boundary, based on a climatic sta-
tion at Cameron (53°40°S, 69*53'W), is 503 mm
with more than 50% of iaa falling in sum-
mer. In the windy, arid climate of inland Tierra del
Fuego (based on field observations from 1995,
1996, 1997),
above the tree line on Cerro Riñón every year for
five months (May through September). Mean annual
temperature at Pampa Guanaco (200 m a.s.l.) lo-
cated some 19 km west of Cerro Riñón is 2.7°C,
while mean monthly temperature during the late
spring to late summer (October-April) is ca. 6.0?C.

and permanent snow was present

SEED SOURCES

Bulk seed collections were made on Cerro Riñón
during March 1996. Species included perennial
herbs, cushion species, shrubs, and one annual-
biennial herb. The choice of species was made so
as to maximize the taxonomic coverage of a man-
ageable number of species, while at the same time
representing a mixture of dominant and subdomi-
nant taxa. Mature seeds at the point of being dis-
persed or seeds recently dispersed around a mother
plant were collected from some 30 or more individ-
uals. When we collected seeds on the soil surface
or lodged within the foliage of a mother plant, we
made a special effort to distinguish between the
current and earlier years’ seeds. The field seed col-
lections were carefully checked under a binocular
microscope for the presence of any aborted and im-
mature seeds, the latter being discarded. Adequate
amounts of filled seed were amassed for 15 species
(Table 1). For each species, 30 seeds were random-
ly selected and measured under the binocular mi-
croscope in order to obtain their lengths and

Volume 91, Number 2
2004

Arroyo et al.
Seed Bank Formation

۹

PUERTO
NATALE
-52°

d
N

'
p
(Jiane | DUNGENES
i
тА
e
>
v n Т.
> ”
2 SAN o
т SEBASTIAN
ч
o т ^
0 E 7
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m Q LYNCH
i «
549 У Z SLA 6
2 LAREN PTO.ARTURO "
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Figure 1. Location of Cerro Riñón in central Tierra del Fuego, Chile.

widths; after that seeds were weighed in a digital
balance (OHAUS). In species with extremely small
seeds (e.g., Calceolaria biflora), these were weighed
in groups of 20 seeds each.

ithin 1 to 2 days of collection in the field, 50
seeds of each species were subjected to the Tetra-
zolium chloride test (Moore, 1973) in order to as-
sess their initial viability.

Over the period 12—14 March 1996 three sets of
six batches per species of 30-39 seeds (total of 18
batches per species) were counted out and intro-
duced into 10 X 10 cm nylon mesh envelopes of
three sizes, electing a smaller mesh size than the
introduced seeds. The envelopes containing the
seeds for each of the 15 species were separated into

three sets, each of six replicates. For every set of

species in a given replicate, the species was as-
signed a number between 1 and 15 randomly, for
later positioning in the buried seed cages.

SEED BURIAL

On 15 March 1996 seeds were transported back
to the field to a burial location on a southeast-facing
slope at 550 m, where six randomly placed repli-
cate burial sites within an area of approximately 50
X 50 m were previously established. The general
burial area, which was flatter than the surrounding
slopes on average, was dominated by Bolax gum-
mifera and Azorella lycopodioides with some lichen
and moss growth at the soil surface, good soil de-

velopment, and moderate drainage. At each of the

Annals of the
Missouri Botanical Garden

Seed shape
achene asymmetrically ovate

navicular, reticulate
ovoid, ellipsoid
ovoid, smooth
achene cylindrical

ovoid
ovoid

cupule obconical
ovoid

lunate, smooth

ovoid
cylindrical

Width
(mm)

Length
(mm)
5.0

shrub.
Weight
(mg)
0.03
0.33
0.15

Life-form
PH
PH
PH
PH
SH

Family
Ranunculaceae
Asteraceae

cushion-forming perennial herb; SH
Rosaceae

perennial herb; CU

Life-form and seed characteristics of the species studied in assessment of potential persistent seed bank formation in the alpine zone on Cerro Riñón, Tierra del Fuego.
Species

annual to biennial herb; PH

Table 1.

Gentianella magellanica (Саа) Fabs ex D. M. Moore

Senecio magellanicus Hook. & Arn.

Acaena ovalifolia Ruiz & Pav.
Anemone multifida Poir.

A-B

six replicate sites, three rectangular areas separat-
ed by 5-10 cm of untouched turf were excavated
to allow for the introduction of three wire cages (70
cm long X 40 cm wide X 5 cm tall). A layer of
sieved soil was placed in the open cages after they
had been introduced into the burial sites. One en-
velope of seeds per each of the 15 species was
placed over the sieved soil, respecting the previ-
ously established randomized order. The seed en-
velopes were covered with additional sieved soil,
and the cages carefully adjusted in the ground such
that the envelopes lay 5 cm below the soil surface.
Roach (1983) found that the great majority of the
seeds fail to penetrate further than 5 cm depth in
soil of arctic and alpine sites. The cages were wired
closed and covered with additional sieved soil and
the original excavated turf, which had been carved
thinner so as to lie at the level of the surrounding
vegetation. The wire cages served to prevent any
downslope movement of the seed envelopes and as
deterrents for the small burrowing mammal Cteno-
mys magellanicus, which has been observed by us
to occur above tree line on nearby mountains in
Tierra del Fuego. The position of each replicate
burial site was marked, and the three cages per
each of the six burial sites identified as to number.
We randomly assigned positions 1—3 to each of the
three cages at each of the six sites for later exhu-
mation on three separate dates.

RETRIEVAL OF BURIED SEEDS
In accordance with the previously randomized
order for retrieval, at each replicate site a set of six
cages was exhumed on the following dates: (1) 14
February 1997; (2) 14 March 1997; (3) 10 April
1998. The first exhumation date was planned so as
to be fairly sure that any current years seed ger-
mination taking place after the winter period would
ave already occurred. The second date was
planned toward the end of the summer-autumn
season so as lo assess the viability of any remaining
seeds after one year's burial and to assess any late
summer seed mortality. The third date was planned
so as to allow the seeds to remain in the soil for at
least 2 full calendar years, thus allowing us to judge
the potential for the formation of a persistent seed
bank. Remaining intact ungerminated seeds re-
trieved on each of the exhumation dates were sub-
jected to the Tetrazolium chloride test, using the
same protocol as outlined earlier so as to determine
the seed viability.

DATA ANALYSIS

The recovered intact seeds demonstrated as vi-
able on the basis of the Tetrazolium test, expressed

Volume 91, Number 2 Arroyo et al.
2 Seed Bank Formation

А 4.5
98.6 + 1.3
94.0

]

as a percentage of initial buried seed number, pro- 3
vided a measure of the “potential” persistent seed EE. EN
2 * +оо Lom
bank (Zhang & Maun, 1994). To assess loss of total S N S
A А . ow
viable seeds over time (and hence depletion of the oe TW E LAA
| | n буо
potential soil seed bank) and estimate maximum Wirt поо
| : о: с |обо más
seed ages, we used the negative exponential model e
= © b
(Guariguata & Azocar, 1988; Lonsdale et al., Й " 3
n . ف4‎ > ‘ te)
linearized for statistical application: In М, = In N, ~
— kt, where N, = mean number of viable seeds at —
time t days; N, = mean initial number of viable Mr. à: РА
' = . ү "olo Ld dh o
seeds. The accepted significant level for the linear z „„ —
i ) ; 8 ‘ao | +1 +1 +1 +I +I HH
regressions was P < 0.05. The age of the last viable = E S | аи
: Р 2. а= | л кб с =
seed for a species was determined by the equation E 2 5 R SE
t = In №. " EE |
Relationships between seed persistence and seed — 7
size and shape were assessed through linear re- d =
" — un
gressions between the percentage of ungerminated — 3 Е
seeds after 2 years’ burial (arcsin transformed for E 9 *
к E . * . 3 © [5] NO U91 p)
normalization) with the seed weight (log trans- 2 аиын | HHH
formed) and the quotient width/length as suggested E an e
app у : $ SSC soa
in Schwienbacher and Erschbamer (2001). zd 2S е ARA соо
EN бе]
©
8 a
эте 2
RESULTS B |2
= (3
Seeds of most of the study species were very J 1519 e -" B
^ І 4 І CES € | сыс
small. Seed size ranged from 1.3 mg weight, 4mm c 2 5 јочоото т
é š Р 3 Р T = + +
long, and 2 mm wide in Senecio magellanicus, to P ES " к А : T uds
Ж Y 9227 22235
0.03 mg, 0.7 mm long, and 0.3 mm wide in Cal- % . SSS шше
B . 9
ceolaria biflora (Table 1). The most common seed = -——
shape was ovoid, followed by cylindrical achene z
(Table 1) ©
. . . КЫҢ. — —
The percentage of viable seeds in relation toini- & —
Р : . „ Ф
tial buried seed number (Table 2) reveals a wide = 2EloaXwone
range of situations among the 15 species studied E .
after being buried 2 years. By the end of the 2-year 8 ә Е bi n п = 1 _ jis
: bes © a юю
period, not a single seed of Acaena ovalifolia, Cal- 5 2 E E APENAS
B . А ы e
ceolaria biflora, Caltha appendiculata, Luzula alo- = || £ =
pecurus, or Azorella lycopodioides had germinated $ | =
or decayed. For these same species, terminal seed = ||%
viability as deduced from the Tetrazolium chloride E E -
А А 13.2
test was over 80%, and indeed close to 100% in a 4 alsz us
"uw" x з 5 8888888
number of cases (Table 2). Similar, but less rigid. 5 = a " pops
. А . o 2
behavior was seen in Anemone multifida and Gen- E 8 3 8882828
Е . к 5р S © )
tianella magellanica, where a small percentage of = E с S S =
А . . Ф
the buried seeds had either germinated or were de- Ф р
cayed, with again a very high percentage of the F
remaining ungerminated seed fraction. remaining E
: s ; : 5
viable (Table 2). For a third group of species, com- zx
posed of Gunnera magellanica and Pernettya pum- ® 5 S
; : 3 5
ila, around half of the seeds had germinated after 3 "V RTI
s . v Ns e 5 Spm S =
the 2-year burial period. However, remaining seeds Ӯ E S `5 SESS
" ya К . qe Д a | ee SS E
continued to exhibit high viability. In three species A 9 S 88 E 8 S
| | $n SES
(Bolax gummifera, Draba magellanica, and Empe- « | Э Š 8 2 mS ы
i Ta = 8
trum rubrum) around % to % of the seeds had exited s S FEES 333
es E
the seed bank through germination or other causes چ چ‎ 4 û & © ©

98.9 + 1.0

46.9 + 16.8
0+0

36.8 + 2.5
50.9 + 8.3
100 + 0

+29

.0 E
98.2 + 1.
TB 28

25.3 + 3.6
100 = 0

85.0 + 4.7
93.6 + 5.9

16.3

Ru

73.8 + 6.6

53.7

5.8

93.9 + 3.1
A

Draba magellanica
Empetrum rubrum
Gentianella magellanica
Gunnera magellanica
Luzula alopercurus
Pernettya pumila
Senecio magellanicus

362

Annals of the
Missouri Botanical Garden

Tierra del Fuego, 54°S, as adduced from seed burial experiments. Species are arranged according

Table 3. Potential to form a persistent seed bank in the subantarctic alpine zone,

ersus a transient seed bank. Species showing potential to form a persistent seed bank are arranged along a gradient from long to

to their potential to form a persistent seed bank v

short persistent seed banks.

Transient seed banks

Short

< Persistent seed banks >

Long

Berberis buxifolia

Oreomyrrhis hookeri

Bolax gummifera

Anemone multifida

Gentianella magellanica

Gunnera magellanica

Acaena ovalifolia

Senecio magellanicus

Draba magellanica
Empetrum rubrum

Pernettya pumila

Caltha appendiculata

Luzula alopecurus

Azorella lycopodioides

Table 4. Significant adjustment (P < 0.05) to the neg-
ative exponential model for loss of viable seed with time
in species from subantarctic alpine zone in Tierra del Fue-

ма
8

go, 5
Predicted
maximum seed
Species n? longevity (days)
Draba magellanica 0.874 1623
Empetrum rubrum 0.881 2
Gunnera magellanica 0.932 3026
Oreomyrrhis hookeri 0.923 777
Pernettya pumila 0.890 5983

within 2 years, with less than % of the original seed
number remaining viable. In the remaining species
(Oreomyrrhis hookeri, Berberis buxifolia, and Sene-
cio magellanicus) no seeds remained intact and vi-
able after 2 years. In O. hookeri, although a fraction
of the seed (2596) had not germinated and remained
highly viable at the end of the first summer season,
none remained in this state by the end of the sec-
ond autumn. In Berberis buxifolia and Senecio ma-
gellanicus practically all seeds had germinated or
had decayed by late summer the first year, and all
had germinated or decayed by the time a full cal-
endar year had expired. Summarizing these results
(Table 3), 13 species (8796) on the subarctic alpine
site showed some potential to form a persistent seed
bank, with seven showing no decay on seed viabil-
ity after 2 years’ burial.

Table 4 shows the species with viable seeds after
2 years’ burial in which there was a statistically
significant fit for number of viable seeds over time
with the negative exponential models. We only ob-
tained significant fits for five species, where esti-
mates of the longevity of seeds buried for these
species revealed a range from 16.4 years (Pernettya
pumila) to 4.2 years (Draba magellanica). We failed
to obtain significant fits in other species because
percent viability in residual physically intact seeds
among the three exhumation dates showed that
there were statistically higher terminal viability
(755 days' burial) in relation to seeds exhumed in
early autumn the previous year (363 days’ burial).
This was the case of Gentianella Mai
Anemone multifida, Caltha appendiculata, and L
zula alopecurus. Suc
ically less apt (more prone to loss of viability) seeds
were more abundant among the intact seeds at the
ume of the earlier exhumation date and had been

a result could accrue if 97

progressively weeded out with time. However, the
percentage of seeds in the germinated and decayed
category stayed relatively constant in these same
species over time, such that there was little change

Volume 91, Number 2
2004

Arroyo et al.
Seed Bank Formation

363

in the proportion of intact seeds over the 2-year

period (Table 2). One-Way ANOVA performed with
aresin transformed for percentage of seed remain-
ing intact showed no significant differences in A.
multifida (F = 1.663, NS), C. appendiculata (F =
1.000, NS), and G. magellanica (F = 2.411, NS
throughout the length of the experiment. A similar
result was obtained in 0. hookeri (t = 0.9204, NS).
The percentage of intact seeds in L. alopecurus re-

м

mained at 100% over the entire experimental pe-
riod (Table 2).

Linear regresssions showed that neither seed size
nor seed shape were significantly related with the
percentage of seeds that remained ungerminated af-
ter 2-year burial. That is, among the studied spe-
cies, independent of the seed size and shape, a high
percentage of seeds remained ungerminated in the
soil after 2 years’ burial.

DISCUSSION

As far as we are aware, our study would appear
t
study for an alpine habitat in which a taxonomically

~

> constitute the first experimental seed burial

diverse set of species (representing 15 genera and
12 families) has been studied simultaneously and
under identical conditions for more than one year.
Including the marginally persistent seed bank spe-
cies, Oreomyrrhis hookeri, we have found that 87%
of the species studied showed potential to form a
persistent seed bank because they maintained an
important fraction of viable ungerminated seed after
2 years’ burial. If we consider that the total number
of species just above tree line in the alpine region
of Tierra del Fuego is ca. 25—30 species (Mark et
al., 2001), according to our results at least 50%
have the potential to form a persistent seed bank.
Thus, considering the definition of persistent seed
bank, our results suggest a fairly generalized po-
tential for persistent seed bank formation in the
subantarctic alpine habitat, with significant seed
longevity in a number of species.

Results obtained for alpine and arctic habitats
with the use of the soil core method have found a
variety of results in terms of percentage of species
present in the persistent component of the seed
banks. For instance, Roach (1983) found 5 out of
б, and 13 out of 35 species represented in the
standing vegetation to be present in the persistent
seed bank at two tundra sites in the Brooks Range,
790 m in Alaska (68°20°N). Ebersole (1989) stud-
ied four tundra communities at Oumalik (69°N) on
the edge of Alaska's Arctic Coastal Plain, and reg-
istered persistent seed banks for 37-58% of the
species in the surrounding vegetation. Ingersoll and

Wilson (1993) studied a treeless high subalpine site
on Mount Jefferson (44°45'N) in Oregon, reporting
a persistent seed bank comprised of 12 (55%) of
the 22 standing vegetation species. Arroyo et al.
(1999) detected persistent soil seeds representing
n the standing vegetation al a
high alpine site (3250 m) in the central Chilean
Andes.

31% of the species i

Percentages of persistent seed bank species ob-
tained with the soil core method are generally lower
than found in the present experimental study. The
fewer persistent seed bank species detected in gen-
eral surveys with the soil core method may partially
be a result of a high probability of missing rare
species in the persistent seed bank. It should also
be borne in mind that in our study, burying seeds
5 em beneath the soil surface might be somewhat
artificial in terms of light penetrance, nutrients, and
drainage. Roach (1983) found a striking reduction
in seedling emergence comparing the second and
first 5-cm layers of soil in Alaskan tundra, sug-
gesting that the great majority of the seeds fail to

E

penetrate further than 5 As Chambers et al.

(1991) pointed out, however, seed entrapment in

cm.

alpine areas is highly dependent upon such factors
as particle size, soil porosity, and seed size itself.
In general, substrates in the South American Andes
are strongly porous with much coarse material
found at the surface as a result of wind erosion,
which, added to the small size of seeds found in
this study, could favor the formation of persistent
seed bank in this habitat

Exclusion of predators in our experimental buri-
als could also be an additional contributory factor
for the difference, although no evidence of burrow-
ing animals was seen at the particular site. By ex-
cluding large seed predators, we have possibly
overestimated real species richness in relation to
the local persistent soil seed bank.

While alpine seeds may remain viable for long
periods under cold laboratory storage conditions
(Billings & Mooney, 1968; Chambers, 1989), little
comparative data are available on seed longevities
in the natural habitat. The prolonged seed longev-
ities predicted on the basis of our experiments thus

very interesting. Using a similar extrapolation
tec етше and the same negative exponential model
we have employed here, Guariguata and Azocar
(1988) estimated that seeds of the giant tropical
Andean rosette species Espeletia ашын could
potentially remain viable in the soil for 4—5 years.
Chionochloa macra turned out to have а non-per-
sistent seed bank in the alpine region of New Zea-
land (Spence, 1990). Cavieres and Arroyo (2001)
reported that in the Andes of central Chile, seeds

Annals of the
Missouri Botanical Garden

of the perennial herb Phacelia secunda remained
viable in the soil for more than 3 years, estimating
a longevity of 1782 days (> 4 years) in seeds bur-
ied at 3400 m a.s.l. The maximum predicted ages
for seeds of several Tierra del Fuego alpine species
fall well beyond that of E. timotensis and P. secun-
da. However, species with shorter longevities were
also revealed for our site.

It should be recalled that mathematical fits were
only possible for 4 of the 12 species showing po-
tential to form a persistent seed bank. Most of those
excluded belong to a group of species in which per-
cent seed viability in the penultimate exhumation
date was significantly lower than on the last date,
resulting in U-shaped seed viability curves. Not-
withstanding, it also turns out that several of the
same species in the group that showed anomalous
behavior in the Tetrazolium test showed little or no
depression in final total viable seeds as measured
on the final exhumation date. Consequently, the
maximum seed longevities estimated on the basis
of curve fitting are probably lower than in several
species for which curves could not be developed.

That significant reductions in viability of physi-
cally intact seeds were registered mostly on a single
observation date (363 days) might indicate a tech-
nical problem. However, this is unlikely because
many species assayed on that date were not affect-
ed, and the experimental protocol was identical for
all species. It is well known that some seeds ex-
perience an annual dormancy cycle when buried
(Baskin & Baskin, 1998) involving profound chang-
es in seed physiology. Changes in basic seed phys-
iology over an annual cycle determining variation
in sensitivity to the Tetrazolium test could also be
expected. The depression in seed viability regis-
tered on the second exhumation date, which was
the driest of the three exhumation dates, followed
by recuperation of the viability reaction at the later
autumn date, is perhaps determined by some aspect
of seed physiology eliciting the Tetrazolium reac-
tion that might be altered by late summer—early
autumn environmental conditions.

One aspect that cannot be evaluated satisfacto-
rily on the basis of the present information is po-
tential phylogenetic effects. A growing body of ev-
idence has demonstrated strong phylogenetic
constraints in flowering phenology (Kocher & Han-
del, 1986), fruit traits (Herrera, 1992), seed number
and mass (Mazer, 1989),
(Thompson et al., 1998).
tried to avoid the confounding effect of possible

and seed longevity
Nevertheless, we have

phylogenetic constraints on seed longevity in our
study by eliminating taxonomic redundancy as
much as possible without compromising the need

to include the dominant alpine species on the study
site. Our data set has no taxonomic redundancy at
the generic level, and only two sources of redun-
dancy at the familial level, where the Apiaceae are
represented by three genera (Bolax, Azorella, and
Oreomyrrhis) and the Ranunculaceae are repre-
sented by two genera (Caltha and Anemone). Pe-
rusal of the results suggests that the seed longevi-
ties of representatives of Apiaceae are almost as
diverse in their seed bank characteristics as the
total set of genera considered. The representatives
of Caltha and Anemone, nevertheless, show fairly
similar behavior.

Finally, although it is clear that there are still
many unknowns surrounding the persistent seed
bank biology in alpine habitats in general, our re-
sults suggest an important potential to form long-
term. persistent seed banks (cf. Thompson et al.,
1998) in many species of the alpine region of the
subantarctic zone of southern Chile. This is in
agreement with recent studies (e.g., Cavieres,
1999), which suggest that factors such as the strong
inter-annual variation in the length of growing sea-
son and the small-scale disturbances in the soil will

LS

avor the formation of persistent seed banks in al-
pine habitats (see also Forbis, 2003). Additionally,
the low diversity of both seed predators and path-
ogenic fungi (McGraw & Vavrek, 1989), and the
ambient low temperatures that are associated with
low embryonic metabolic rates and slow consump-
tion of seed reserves, favor the seed longevity ob-

served in alpine soils.

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Potential for seed bank

366 Annals of the
Missouri Botanical Garden

STATISTICAL SUMMARY OF SOME OF THE ACTIVITIES IN THE MISSOURL BOTANICAL GARDEN HERBARIUM, 2003

Vascular Bryophyte Total
Acquisition of Specimens
Staff Collections 24,234 2,526 26,760
Purch 0 0 0
Exchange 16,207 2,865 19,072
Gifts 5,205 156 5,411
Total acquisitions 45,696 5,947 51,243
Mountings
Newly mounted at MO 99,505 24,355 123,920
Specimens mounted when acquired 31,382 n/a 31,382
Repairs
Specimens repaired 18,183 n/a 18,183
Specimens stamped 1.375 n/a l 555
Total repairs 19,558 n/a 19,558
Specimens Sent
On exchange 27,340 489 27,829
As gifts 14,520 1,088 15,608
Total 41,860 1,577 43,437
Loans Sent
Total transactions 256 35 291
Total specimens 23,850 1,816 25.666
To U.S. institutions
Transactions 144 16 16(
Specimens 14,144 284 14,428
To foreign institutions
Transactions 112 19 131
Specimens 9,706 1,532 11,238
To student investigators
Transactions 36 3 39
Specimens 5,109 102 5,211
To professional investigators
‘Transactions 220 32 252
Specimens 18,741 1,714. 20,455
Loans Received
Transactions 184 36 220
Specimens 13,171 6,304. 19,475
From U.S.A. From abroad Total
Visitors 248 157 405

During 2003, 155,302 specimens were accessioned into the herbarium: 123,920 mounted at MO, 31.382 тше
when ас quired, and 1,375 old MO specimens stamped (and numbered). The total number of mounted, accessioned
spec imens in the herbarium on 1 January 2004. was 5. 518.588 (5,087,212 vascular plants and 431,376 bryophytes),

The 31,382 vascular plants listed as “mounted when acquired” are all from the Reed Herbarium, purchased in 2001,
and represent about 20 percent of that acquisition

Volume 91, Number 2 Crosby & Solomon 367
Statistical Summary

rden’s herbarium is closely associated with its database management system, TROPICOS (see (www.mobot.
буйи оше h)). The charts below summarize some of the statistics from TROPICOS both for an calendar year
003 and as year-end totals. Note that the specimen records in TROPICOS are primarily based on MO specimens,
meaning that about forty-one percent of the bryophytes (an increase of about three percent over 2002) and thirty-five
percent of the vascular plants (an increase of about two percent) in the herbarium are now computerized, with an
overall total of about thirty-six percent (an increase of about two percen

TROPICOS records—Calendar Year 2003 Additions

Bryophytes Vascular Plants Total
Specimens 18,937 129,805 148,742
Names 2,499 20,570 23,069
Synon 1.376 10,313 11.689
Distributions ATT 24,889 25,306
es 736 12,765 13,501
Bibliography 1,393 3,857 5,250

TROPICOS records— Year-End 2003 Totals

Bryophytes lascular Plants Total
Specimens 175,553 1,789,622 1.965.175
ames 106,132 833,232 939.364
Syno 69,63 | 416,862 486,493
Distr ‘butions 43,297 848,052 891,349
ypes 9,630 304,386 314,016
Bibliography 26.449 70,829 97,278
Specimens in herbarium 431,376 5,087,212 5,518,588

Percent of specimens

computerized 41 35 36

In TROPICOS, literature-based Synonymy is always linked to a reference in Bibliography and directly with at least
the synonym, often a basionym, and the correct name according to the reference. Additional

two records in Names,
e.g., all other combinations of a basionym treated as a synonym of

synonymy may be derived from these direct links,
a given name are also synonyms of i

—Marshall R. Crosby and James C. Solomon

Volume 91, Number 2, pp. 225—368 of the ANNALS OF THE MissoURI BOTANICAL GARDEN
was published on July 13, 2004

isso tanical Garden Libr.

ШИ

00318 3396

www.mbgpress.org

CONTENTS

Revisión Taxonómica del Género Paspalum Grupo Eriantha (Poaceae, Piuitoideas,

ahiceae]) . сс Osvaldo Morrone, Silvia S. Denham & Fernando O. Zuloaga
Phylogenetic Analysis of the Madagascan Euphorbia subgenus Lacanthis Based on ITS
Sequence Data Thomas Haevermans, Petra Hoffmann, Porter P. Lowry П,

Jean-Noél Labat & Emile Randrianjohany

Hooglandia, a Newly Discovered Genus of Cunoniaceae from New Caledonia —
Gordon McPherson & Porter P. Lowry П

Phylogenetic Position of the New Caledonian Endemic Genus Hooglandia (Cunoniaceae) as

Determined by Maximum Parsimony Analysis of Chloroplast DNA
Patrick W. Sweeney, Jason C. Bradford & Porter P. Lowry II
Evolution of Veroniceae: A Phylogenetic Perspective Dirk C. Albach,

Ma. Montserrat Martínez-Ortega, Manfred A. Fischer & Mark W. Chase |

Cladistic Relationships of е (Bromeliaceae; Bromelioideae) and Allied Genera
а Paula Gelli de Faria, Tania Wendt & Gregory К. Brown
What Is the Taxonomic Status > skiepai Evidence of Floral Morphology ...
L. P. Ronse De Craene, S.-P. Hong & E. E Sad
. Pollination Biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico
K. S. Burgess, J. Singfield, V. Melendez & P. G. Kevan
Experimental Evidence of Potential for Persistent Seed Bank Formation at a Subantarctic
Alpine Site in Tierra del Fuego, Chile
Mary T. Kalin Arroyo, Lohengrin A. Cavieres & Ana María Humaña
Statistical OMENS of Маке: of the Activities in the Missouri Botanical Garden Herbarium,
Marshall R. Crosby & James C. Solomon

v | Cover illustration. Trisetum ligulatum Finot & Zuloaga, drawn by Vidas Dudás.

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Volume 91 Annals
Number 3 of the
2004: ISSOUTI

otanical
arden

POLLINATION ECOLOGY OF Richard R. Clinebell Il. Angela Crowe,”
GAURA AND CALYLOPHUS David P. Gregory," and Peter C. Hoch?
(ONAGRACEAE, TRIBE

ONAGREAE) IN WESTERN

TEXAS, U. S.A.

ABSTRACT

This analysis reports insect visitors, with pollen load data. for the major i ring species of a plant community al
the Monahans Sandhills and nearby sites in the Transpe cos region of western Texas, U. S. A., with concentration on four
species of Onagraceae, tribe Onagreae. We characterize the pollinators of two species of Gaura (G. coccinea and €
villosa) ма two species of Calylaphas (C. berlandieri and C. hartwegii), as well as three major co- ине non-onagr "id
specie Dl ag ooo (Asteraceae). Mentzelia strictissima (Loasaceae), and Argemone polyanthemos

were collected on two additional species of Onagreae, Oenothera engelmanii and O.
po ae collections were made during repeated visits to the plant community, with sampling throughout
24-hour pe riod. Nearly 1300 insects were captur red on the nine target plant taxa, with more
of Onagraceae studied had diverse insect visitors, and

veraceae)). Partial «

e flowering season and a
mh 100 insect species carrying pollen. The primary species
n as 3 Lee carriers for different species. Gaura villosa showed the greatest diversity,

2 д cies of noctuid

different insects ser
with at least 32 insect species carrying pollen, the major carriers being the antlion ез
moths, and 2 halic e ене іп ан By contrast, the pollen carriers of G. coccinea we

moths: of Calylophus berlandieri one of the same species of Sphecodogastra, several chrysome did 2 нен. beetles

uid and geometrid

The authors are grateful to Peter H. Raven and Dennis Breedlove for э opportunity to study and analyze their
earlier collections of onagrad pollinators for inclusion in this paper and to the National Geographic Society and the
Missouri аш ‘al Garden for fieldwork support. We also gratefully ac (nm dge prior support for Raven from the l
National Science Foundation. We are grateful to the Field Museum for funding research at the Museum by Clinebe l
and for 5 to work with their collections. We thank the following taxonomic specialists for help with insect
: Ted MacRae (Monsanto Company) ) and Philip Parrillo (Field Muse um) for Coleoptera: Neil Evanhuis
(Bishop Museum) and David Pollock (Bishop) for Diptera: Mike Arduser (Missouri Department of Conservation) and
Ron MeG inley (Illinois Natural History Survey) for Hymenoptera: Paul Goldstein (Field), Phil Koenig (no affiliation),
and Richard He бе (no affiliation) for Lepidoptera: and Norm Penny (California Academy of Sciences) for Neuroptera.
CH). Warren Wagner (US). and George Yatskievych (MO) au a he ip with plant identifications.
and ате son docu-

Robert Raguso (US
Don Hardin (Washington University) provided assistance in the field, prepare Wo of tables,

mentation. Richard Keating (MO) helped in the pre d A of photomic rographs. We are grateful to the library staff of
the Missouri Botanical Garden for their generous help in locating and borrowing necessary e nome al public ations.
We also thank Raguso, the editor, and an anonymous re viewer for comments that dei Л this pay

? Missouri. Botanic: sl Garden. P.O. Box 299, St. Louis. Missouri 63166-0299, U.S.A. shard р е ТИРЕ Ч org:

3 ' Fouthonne College. St. . Miss
24 Baldwin Court, E New ое 03447, U.S.A.

ANN. MISSOURI Bor. GARD. 91: 369—400. 2004.

Annals of the
Missouri Botanical Garden

(Coleoptera), and several beeflies (Diptera); and of C. hartwegii a combination of the sphingid moth Hyles lineata,
The

several noc jm M the hone ybee | Apis mellifera, and the same species of Sphecodogastra.

ey: had a div

1 Onagraceae anc ni the non-onagrads. This re port of pollination by antlio

member of the order Neuroptera. At least 5 species of а
minusculus is the most important pollen-carrying specie
10:00 р.м. and 5:00 a.M., which may explain why

Key words:

7
7
5
=
Y
=
=
=
3
=
=
—
a 03
a 2
7
Y
=
—
=
—
=
%
=
©
=
—
=
=
E
=
=
=
—

intlions vis | the flowers of sa, and Scotoleon
s for this taxon. АП visits b petit occurred between

this ы nomenon has not been reported before.
antlions, Calylophus, Gaura, Onagraceae, pollination, Sphecodogastra.

The plant family Onagraceae provides an excel-
lent model in which to study the evolution of pol-
lination systems. Due largely to the efforts of Raven
(1979, 1988) and associates, detailed modern tax-
onomic revisions are available or in preparation for
virtually all species of the family, as are detailed
comparative studies of the morphology and anatomy
of pollen, stigmas, flowers, seeds, and other repro-
duc (a с 7 ‘ters (reviewed in Raven, 1979; Hoch
et al., 1993). At least preliminary pollination data
have published for many groups, especially
Oenothera (Gregory, 1963, 1964, including Caly-
lophus: Linsley et al., 1964), Camissonia (Linsley
et al., 1963a, b, 1973; Raven, 1969), and Clarkia
(MacSwain et al., 1973) in the tribe Onagreae, and
Raven (1979) presented a lucid overall synthesis of
the reproductive biology of the family. Recent work
by Raguso and associates (Raguso & Pichersky,
1995; Raguso & Willis, 2002; Levin et al., 2003a)
has begun to document adaptive changes in nectar,
floral morphology, visual display, and floral fra-
1

—

grance associated with hawkmoth pollination i
Onagraceae and other families, building in part on
earlier studies by Gregory (1963, 1964

An understanding of relationships within Ona-
graceae (8 tribes, 17 genera, and about 650 spe-
cies; Raven, 1988; 2003b), which is

essential to a comparative study of pollination bi-

Levin et al.,

ology, is beginning to emerge. based on both mor-
1993) and molecular phy-
logenetics (Crisci et al., 1990; & Zimmer,
1993; Conti et al., 1993; Levin et al., 2003b, 2004).
Of particular importance to the present study is the

phological (Hoch et al.,

strong support for a terminal clade that includes
tribes Onagreae (8 genera) and Epilobieae (2 gen-
era; Conti et al., 1993; Levin et al., 2003b). Raven
(1964) suggested that Gaura and Calylophus, two
genera of Onagreae, were closely related based on
similarities in stigma and anther morphology, a
view supported by embryological studies (Tobe &
Raven, 1985). Recent phylogenetic analysis of On-
agreae based on chloroplast and nuclear DNA se-
quences (Levin et al., 2003b, 2004) strongly sup-
ports a clade of Calylophus + Oenothera + Gaura
+ Stenosiphon, and a close sister-taxon relationship

between Gaura and Stenosiphon, the latter clade
also supported by Hoggard et al. (2004). However,
Calylophus now appears to be more closely related
to certain sections of Oenothera, and the Gaura +
Stenosiphon clade to other sections of Oenothera.
Additional study is in progress, using additional
nuclear DNA sequences and more extensive sam-
pling within the tribe, since these initial findings
challenge the classification of the tribe that has
been in place for some 40 years (Raven, 1964,
1979, 1988).

Gaura (21 species; Raven & Gregory, 1972a, b)
and Calylophus (6 species; Towner, 1977) both oc-
cur primarily in the southern plains of the United
States and adjacent Mexico, with concentrations of

—
—

taxa in western Texas. Morphological (Carr et al.,
1990) and molecular (Hoggard et al., 2004) phy-
logenies for Gaura are available; those for Calylo-

—

phus are in progress. Both genera are characterized
by a diversity of pollination systems. Five species
of Gaura are reported to be self-pollinating, and of
the 16 outcrossing species, 13 are pollinated by
small moths, | by hawkmoths, and 2 by bees, but-
terflies, and flies (Raven & Gregory, 1972a; Raven,
1979). One species of Calylophus is reported to be
autogamous, and of the five outcrossing species,
three are visited by hawkmoths (one of these also
by various bees), and the other two by bees, beetles,
butterflies, and ни hawkmoths (Towner,
1977; Raven, 1979), The diversity of pollination
syndromes found in s genera provides testable
hypotheses regarding the evolution of the species
and their reproductive biology.

Even in this comparatively well-known tribe On-
agreae, much of the information on pollination sys-
tems is descriptive or anecdotal and often rests on
insect pollinator collections from only one or a few
short periods of observation. Few previous stud-
have docu-

in this or most. other

ies groups
mented insect visitors to a plant species through
the entire daily and seasonal cycles (Robertson,
1928) nor have many tested the efficacy of those
visitors as pollen vectors (Schemske & Horvitz,
1984)

Our study exploits three features of Gaura and

Volume 91, Number 3
2004

Clinebell et al.
Pollination Ecology

]
GAINES DAWSON BORDEN SCURRY FISI
New ANDREWS MARTIN | HOWARD | MITCHELL | МО
o Mexico| | . in —
EL PASO rue T E
Texas | Ñ uU SEER Mp ween
HUDSPETH CULBERSON WARD 9'3 P —
ш REAGAN 7 том
REEVES Pa RE Me | RION |
d ies
‘NS neu |
P d : | SCHLEIC
/ PECOS |
8 JEFF DAVIS D CROCKETT | —
l = | SurTI
== (a \ |
А 2 EM - A —
L30 Chihuahua | No TERRELL |
(M EXICO) PRESIDIO | s VAL VERDE т
BREWSTER
=
|
о 100 km
Coahuila
T (MEXICO) — 192°

Figur May

U.S.A., with adjac
Coahuila): nos 1-9 on map refer to ahidi site poa alites

of southwestern Texas,

Calylophus—the existence of a diversity of major
pollinators, the availability of sound taxonomies
and testable phylogenetic hypotheses, and the oc-
currence of several related plant taxa in a relatively

restricted geographical area—to facilitate the gath-

ering of comparative pollination data and the eco-
evolutionary interpretation of these data. Our ap-
proach simultaneously considers the patterns of
pollinator visitation of several taxa of Onagreae. as
well as that of the major co-blooming taxa in other
plant families that grow with them. This approach
provides data for an entire pollination community,
which in turn will facilitate Comparison with other
communities, for our purposes especially those with
similar clusters of Onagreae.

This paper considers the community pollination
biology of four common and two uncommon sym—

patric species of Onagreae and three important co-

ent sections of New Mexico and Mexico (Chihuahua and
detailed in Table 1

blooming species in Asteraceae, Loasaceae., and
Papaveraceae, in the Monahans Sandhills and sur-

rounding areas in western Texas (Fig. 1; Table 1,
with voucher information). Two other species of On-
agreae, Oenothera engelmannii and O. rhombipe-
tala, were present at the site, but attracted few in-
sect visitors (based on limited observations) and
may be autogamous. Future papers in this series
will include analyses of other communities in the
American Southwest rich in representation of spe-
cies of Onagreae, especially Gaura and Calylophus,
leading ultimately to an evolutionary synthesis for
the pollination biology of these groups. Our primary
focus here is to describe and quantify the pollinator
guilds for a plant community in the Monahans
Sandhills that includes a variety of species of On-
agraceae, as a step toward analvzing the evolution

of pollination biology in Onagraceae tribe Ona-

Annals of the
Missouri Botanical Garden

Table 1
on Figure

Localities included in this study. All sites are in Texas, U. S. A.;

locality numbers coincide with numbers

and are referenced in the text and Tables 4—10. Plant species studied at each locality are noted with

vouchers, where available (all specimens deposited at MO except as noted). Plants are in family Onagraceae, except

as noted.

Brewster Co.: outskirts of Alpine; 2 June 1964

Gaura coccinea Pursh: Raven & Gregory 19182 (CAS)
16.2 km W Marathon on TX Hwy. 90; 22-28 May 2000

Brewster Co.:

Pain. hartwegii (Benth.) P. H. Raven subsp. filifolius (Eastw.) Towner & P. H. Raven: Clinebell 2086

Clinebell 2085
) km E Monahans on TX Hwy.

Gaura coccinea
3. Crane Co.: 20.8 1053:
Gaura villosa Torr. subsp. villosa: Gregory s.n. (RS
4. Ector Co.: 22.4 km E Monahans on US Hwy.
Gaura coccinea: Raven & Gregory 19234
G. villosa subsp. villosa: Raven & Gregory 19235
Ector Co.: 17.2
Gaura coccinea: Clinebell, no voucher
6. Jeff Davis Co.: 9.3 km € 30.4 km S Toyahvale;
Gaura coccinea: Gregory 108-163 (RSA)

Midland Co.: W end of Midland; | June 1964

; Monahans on US Hwy.

. Ward ( S Monahans, 2 June 1964

1-20 ee road;

- rontage road:
1-20 frontag l

16 May

18 June 1966

1-2 June 1964

28 May 2000

1959

Саига d subsp. villosa: Raven & Gregory 19224 (RSA)
7 km

clan regi subsp. filifolius: 7 70 & Gregory, no voucher

Gaura coccinea
9. Ward Co.:
ОО; 6-13 May 2

en & Gregory 19231 (CAS)

2-14 ын ë um on US 11 1-20 frontage road; 7-12 June and 30 Aug-1 Sep. 1999; 20-29 May

Calylophus ien Spach subsp. о ió 2034, 2096

C. hartwegii subsp. filifolius: Clinebell 2093, .
Gaura villosa subsp. villosa: Clinebell 2032, ben
ccinea: Clinebell, no voucher

0e bis ra engelmannii (Small) Munz: Clinebell 2040, 3063

O. rhombipetala Nutt. ex Torr. & А. Gray: Clinebell 2031,

steracea

2041

e: Thelesperma megapotamicum (Spreng.) Kuntze: Clinebell 2033
Loasaceae: Mentzelia strictissima (Wooton & Standl.) J. Darl.:

Clinebell 2039

Papaveraceae: Argemone polyanthemos (Fedde) С. B. Ownbey: Clinebell 2037

sis address-

greae. As an additional focus, our analy
es the debate regarding generalized versus special-
ized pollination, using the community pollination
ecology of the Monahans site.

MATERIALS AND METHODS

The data presented here utilize pollinator collec-
tions made by D. Breedlove, D. Gregory, P. Raven,
and Н. 1959-1966 throughout North
America on Gaura (Raven & Gregory, 1972a, b)
and in the 1970s on Calylophus (Towner,
1977). Many of those results were reported anec-

Towner in
early

dotally in those monographs. One of us (RC) ex-
tended these studies on both genera starting in
1998. We have combined these data sets into sev-
eral biogeographically meaningful units (Table 1),
of which the data set presented here is the first.
Most of the earlier data were collected between
7:00 P.M. and midnight,
lections strongly weighted toward noctuid and

resulting in specimen col-

sphingid moths, which are both active primarily at
dusk. Subsequent observations revealed the impor-
tance of other pollinator groups that are active dur-
ing other times of the day and night. In order to
render the analysis random or unbiased with regard
to time of day, recent fieldwork has emphasized
these other times of pollinator activity, with rela-
lively less sampling from 7:00 P.M. to midnight.
Relative amounts of time devoted to pollinator cap-
ture by time of day are presented in Table 2.
Within any time period, we tried to randomize
sampling of floral visitors in recent fieldwork. The
Insect-capture technique employed multiple nets
and killing jars, each dedicated to one plant spe-
cies. The collector(s) alternated among the different
net-jar combinations, which enabled more or less
continuous collecting, avoided delays while the in-
sects were asphyxiated in the jars, kept the samples
collected on each plant species separated, and re-

sulted more equal sampling times among plant

Volume 91, Number 3
2004

Clinebell et al.
Pollination Ecology

373

Table 2. Cumulative hours spent collecting

pollinators at each plant species by time period and average number

of insects caught per hour of observation. In some cases, we collected insects from more than one plant species during

the same time period, as explained in the text.

Average
# insects

12 A.M. " VM. SAM. 12 rM. 4P.M. SPM. Total caught/
TO ro ro TO ro observation observation
4 A.M. в, . M. 12 рм 4PM. SPM. 12 A.M. 10UrS ho
Gaura villosa 8 15 9 3 9 20 04 8.0
Calylophus berlandieri 8 15 8 6 10 12 59 4.3
Gaura coccinec 2 2 14 18 13.2
Calylophus hartwegii l 2 9 12 0.5
Thelesperma megapotamicum l 3 | 9 l 18 9.4
Mentzelia strictissima 1 6 6 7 23 18
Argemone polyanthemos 4 0 6 7 23 3.1
Oenothera rhombipetala 6 6
Oenothera engelmannii 2 5 2 2 11
Totals 16 42 39 15 44 78 = 234

species. A primary set of insect specimen vouchers
is maintained at the Missouri. Botanical Garden,
with duplicate sets deposited at the California
Academy of Science, the Enns Museum at the Uni-
versity of Missouri, the Field Museum, the Smith-
sonian Institution, and the Snow Entomological Mu-
seum at the University of Kansas. Clinebell visited
the Field and Snow museums to consult their col-
lections.

Pollen load analysis involved bathing the insects
in ethanol, or removing pollen from corbicular or
scopal provisioning loads, and making permanent
slides stained with basic fuchsin (Calberla's solu-
tion: Clinebell & Bernhardt, 1998).

were then identified with the aid of a pollen refer-

Pollen loads

ence library (at MO), consisting of similarly pre-
pared slides for each of the plant species blooming
at the site. Pollen of Onagraceae is highly distinc-
tive due to its shape, “paracrystalline beaded” ek-
texine. and viscin threads (Raven, 1988; Hoch et
al., 1993), and even in mixed pollen loads we were
able to distinguish among specific taxa of Calylo-
phus, Gaura, and Oenothera using pollen size,
shape, and apertural outline, as described by Prag-
(1987,

tables and facilitate comparisons among individuals

lowski et al. 1988). In order to simplify the
and sites, we grouped pollen loads into five size
classes. with the largest being simply “> 500
grains.” In order to calculate total amounts of pol-

len carried by species and overall, we used the
mean of each size class (1.e., 1-10 grains—mean
5: 11-50—mean 30; 51-100—mean 75: 101—
500—mean 300; and > 500—estimate 500), mul-

tiplied times the number of individuals

л
oe

in that
class.

In addition to determining overall pollen load on
individual insects, we tried to note the pattern of
pollen deposition and specifically where on the in-
sect body the pollen was found. Coupled with ob-
servation of insect behavior in the course of floral
foraging, this pattern may provide useful data re-
earding the efficacy of the insect as a pollinator. In
all cases we recorded total pollen present on cap-
tured insects.

In listing Lepidoptera (moths and butterflies) in
our

tables, we have followed most standard refer-

ences on North American moths (Covell, 1984;
Holland, 1968), while acknowledging that the ac-

cepted higher classification of some groups such as
the Catocalinae has been modified quite substan-
1989). According to Hepner’s (1998

classification of Lepidoptera, all of the moths we

tially (Poole,

—

encountered belong to suborder Glossata, cohort
Myoglossata, division Ditrysia. Within this group,
all except the Pyralidae (sect. Tineina) belong to
section Cossina, subsection Bombycina. McGinley’s
(2003) recent monograph of the halictid bee genus
Sphecodogastra proved most useful for that group,
as did Penny et al. (1997) for the Neuroptera
our sample. Determinations for most insect groups

n

were provided or checked by authorities as listed
in the acknowledgments.

The collection protocol, large sample sizes, and
pollen load analysis are intended to ensure that our
methods will include the major pollen carriers for
each species of plant studied. This in turn enables
accurate delimitation of both similarities and dif-
ferences in the pollinator guilds serving each plant
When sufficient data were available,

species. we

tested the statistical significance of pollinator

Annals of the
Missouri Botanical Garden

Table 3. Selected floral characters related to pollination biology for species of Onagraceae in this analysis; mea-

surements (mm) listed are the mean of measurements made on five individuals from the

primary study population.

Measurements in parentheses are from descriptions provided in revisions for Calylophus (Towner, 1977), Gaura (Raven
& Gregory, 1972a), and Oenothera (Dietrich & Wagner, 1988).

Floral tube

istance
Length of е sis Distance
cylindrical Length of Diameter o lon from throat
Taxon part flaring apex at throat peres to stigma Petal length
Calylophus berlandieri 4.8 5.6 7.0 7.8 8.2 15.2
(3-11) (2-9) (3-14) (2-11) (4-10) (6-25)
Calylophus hartwegii 19.2 11.6 5.5 7.6 12.8 12.6
(11-33) (5-17) (4-14) (6-13) (8-12) (12-23)
Gaura coccinea 5.0 N/A 2. 5.0 7.0 5.0
(4-11 Ве = (3-7) (6-10) (3-8)
Gaura villosa 2.4 N/A 2.0 6.9 8.1 4.3
(1.5-5) — (4-11) (7-13) (7-13)
Oenothera rhombipetala 29.0 N/A 5.0 15.0 25.0 20.0
(30-45) = - (13-23) (15-25) (15-35)

choice using Chi-square test. for. independence
(Conover, 1980), where similar pollinators seemed
to be choosing different onagrads to visit in their
foraging activities. The null hypothesis predicts
that insect groups should visit different plants
equally during their respective times of flower-vis-
iting activity.

Behavioral observations are necessary to sepa-
rate those carriers of pollen that might be expected
to effect pollination from those that do not. In terms
of logistics, it is difficult to collect and observe si-
multaneously. While our characterization. of the
pollinator guilds is quantitative, our behavioral ob-
servations are, by their nature, qualitative. Behav-
ioral observations often are sufficient to separate
pollinators from non-pollinators, but may not be
sufficient to evaluate the relative efficacies of var-
ious pollinators. We tried to combine collection and
observation at all study sites.

One challenge in this study is that all groups of

insect visitors are not equally likely to be captured.
In three instances, our field activities unwittingly
baited insects that are included in our data. (1) The
onagrad oligolege Sphecodogastra noctivaga is
largely nocturnal on Gaura villosa, and because
these bees are small and hard to see at night, most
were captured secondarily in net sweeps for moths.
However, Gregory collected a large set of this spe-
cies (including many females carrying onagrad pol-
len) under the dome light of his car while parked
at а Gaura villosa colony in the Monahans Sand-
hills, and we have included these data in our anal-
ysis. (2) Colorful, orange and black beeflies (Poe-
cilanthrax effrenus) are regular diurnal visitors to
both Calylophus berlandieri and Thelesperma me-

gapotanicum, but due to their extremely fast and
unpredictable flight, they are almost impossible to
catch in the act of foraging, and few were actually
captured on flowers. On several occasions, however,
large numbers of these beeflies were captured when
they landed on nets, clothing, and skin, apparently
attracted by a concentration of onagrad secondary
compounds. Most of these insects carried either
Calylophus or Thelesperma pollen, and were as-
signed to these respective species in the tables. The
few beeflies that lacked pollen loads have been as-
signed to Calylophus, since they appear to have
been attracted by volatiles of that species. In gen-
eral, it is our assumption that baiting is a legitimate
part of scientific sampling, especially for document-
ing relative abundances of such a diverse community
of floral visitors as reported here. (3) Whereas five
species of antlions were captured on Gaura villosa
flowers, the only two males of Brachynemurus hub-
bardi were collected at the car dome light. How-
ever, both carried Gaura pollen, so we included
them in our analysis even though they were not
caught actually visiting flowers.

FLORAL FEATURES AND PHENOLOGY

Table 3 summarizes floral measurements of par-
ticular relevance to pollination for the taxa of On-
agraceae in this analysis, with mean measurements
from our study populations as well as overall ranges
of measurements for the species. Five taxa (both
species of Gaura, Calylophus berlandieri, Argemone
polyanthemos, and Mentzelia strictissima) were in
full bloom from early May through early September,
while only a few flowers were present on Theles-

Volume 91, Number 3
2004

Clinebell et al.
Pollination Ecology

Figure 2. Ward Co..

g cun in Monahans Sandhills,
(photo by D. Hardin

perma megapotamicum in late August through early

September. Oenothera were in
bloom on only one of the four field trips to the site
made by Clinebell: Oenothera engelmannii was in

full bloom in early May 2001, and О. rhombipetala
only in early June 1999,

STUDY AREAS

All of our study sites are located in an area
bounded roughly by 30.2-32.1%N, 102-103.8%W, in
Ector, Jeff Davis, Midland.
Ward Counties of southwestern Texas, U.S.A. (

Brewster, Crane, and
\ lable
l; Fig. 1). Our primary sites occur within the Mon-
the

other sites are located in the adjacent Transpecos

ahans Sandhills eco-geographic region (Fig. 2):

region (between the Pecos and Rio Grande Rivers).
Elevations of these sites range from about 800 to
1400 m.

The Monahans Sandhills are a young feature of
the Pecos Plain (about 16,000 years old: Machen-
1984), bordering the Caprock Escarpment
along the western border of the Llano Estacado, or
southern high plains of south-central North Amer-
ica. The sandhills formation extends along this es-

berg,

carpment, which trapped the sand on its leeward
side, about 50 to 100 km east of the Pecos River.
The dune formations extend northwesterly from the

Texas (site 9,

Table 1); typical dune vegetation: | Sep. 1999

km of
southeastern New Mexico, and range from 20 to 60

km across,

Monahans dunefields through about 250

from east to west. Their formation is
associated with paleowinds from the northwest and
the arid. conditions that accompanied the close of
the most recent ice age (Machenberg, 1984).

The preservation of a section of the sandhills for-
mation stems from the publication of Bedichek’s
(1947)
inspired local support for protection beginning in
1957. 5
been preserved as Monahans Sandhills State Park
Ward Co., Texas), which features both active and
stabilized dunes. This park, located about 8 km to
the US
1-20. and its immediate surroundings served as our
l; Fig. 2). Because

the park is closed at night when many onagrad pol-

Adventures with a Texas Naturalist, which

Today, 1554 hectares of the sandhills have

—

west of Monahans bordering Highway

primary study site (site 9, Table

linators are active, our study areas were adjacent
to the park along the frontage roads on both sides
of 1-20.
dunes, which are stabilized by the miniature shin
oak (Quercus havardii Rydb.). Other woody plants
commonly

ese areas contain many fine coppice

encountered include honey mesquite

(Prosopis glandulosa Torr.) and desert willow (Chil-
opsis linearis (Cav.) Sweet). Major grasses include

xeric species of Andropogon, Calamovilfa, Eragros-

376

Annals of the
Missouri Botanical Garden

tis, and Panicum; cacti and Yucca are also abun-
dant (Machenberg, 1984). Embedded in this matrix
is a rich diversity of forbs, of which the species
studied are the most abundant from late May to
early September. Nearby secondary study areas
(sites 3—5, 7—8) are similar.

On a map, the dunal areas appear as islands on
the
species of Onagraceae commonly encountered in-
clude Calylophus berlandieri,

Pecos plains. In the dunal areas themselves,
Gaura villosa, and
Oenothera rhombipetala. On interdunal sites, the
common onagrads are Calylophus hartwegti, Gaura
coccinea, and С. villosa.

ıe sites in Transpecos Texas (sites 1, 2, 6 in
Brewster and Jeff Davis Counties, about. 100 km
southwest of the Monahans Sandhills) include more
arborescent elements of mesquite savanna, and are
rich in Gaura coccinea and Calylophus hartwegii.
Here, the onagrad species typical of the dunes were
absent. Overall, the mosaic character of the sand-
hill belt is such that it is not unusual to find these
key onagrads in various random subsets, depending
upon local variation in substrates. Additional spe-
cies of Onagreae are present in southwestern Texas,
but we believe that the ones chosen for this analysis
represent a majority of the pollination syndromes
of Onagreae that occur in the Transpecos and Perm-
ian Basin (area to the east of the Pecos River, and
of which the sandhills are a part).

RESULTS

Insect visitors were collected throughout the day
and night from nine species of plants in south-
western Texas, including six species of Onagreae
(Tables 1, 2). We present data on Onagraceae first,
followed by other families, and within Onagraceae
list species in order of decreasing size of visitor
samples.
GAURA VILLOSA TORR.

SUBSP. VILLOSA

Gregory studied this self-incompatible perennial
species in the sandhills region (sites 4 and 7 in
June 1964 and site 3 in June 1966). His collec-
tions, made between к 8:00 P.M. and midnight,
are included with Clinebell’s data from site 9 in
1999-2001,

crete time intervals.

which were recorded in additional dis-
Almost every moth collected
at site 4 on 2 June 1964 contained Gaura pollen
on the proboscis, whereas a similar collection of

moths made at site 7 on | June 1964 less than 50
km away contained almost no Gaura pollen; these
latter account for many of the “no Gaura pollen”
individuals of the two most abundant noctuid moth

foragers, Bulia deducta and Melipotis indomita (un-

derwing subfamily, Catocalinae). A collection of 46
pollinators made at site 9 on 30 Aug.-1 Sep. 1999
is combined with data from May to June, since the
two data sets include comparable groups of polli-
nators. We collected additional pollinators at site 9
on 6-13 May 2001. Extreme drought marked the
1999 and 2000, whereas the winter of 2001
was very wet, producing remarkable flowering dis-

years

plays throughout western Texas.

As summarized in Table 4, we captured a total
of 562 insect visitors belonging to 45 species on
Gaura villosa. In terms of individual visits, the 27
species of Lepidoptera account for a majority (353
visits; 63% of the total) followed by the 6 species
of Neuroptera (128; 23%), and the 7 species of Hy-
menoptera (68; 12%): visits by Coleoptera (3 spe-
cies) and Diptera (2 species), mostly without pollen,
are negligible. The most numerous visitors by spe-
cies are the noctuid moth Bulia deducta (253;
45%), the antlion Scotoleon minusculus (104; 18%),
the noctuid Melipotis indomita (46; 8%), and 2 spe-
cies of the halictid bee Sphecodogastra (each 27;
5%). We estimate that these 562 individuals carried
some 32,705

ried, the importance of the Lepidoptera is dimin-

—

pollen grains. In terms of pollen car-

ished relative to the other two groups: Neuroptera
account for gross pollen load of 20,045 grains
(61%), Hymenoptera for 8720 (27%), and Lepidop-
tera for only 4035 (12%). The species that cumu-
latively carry the largest pollen loads are the ant-
lion Scotoleon minusculus (18,160 grains; 55%), the
halictid bee Sphecodogastra danforthi (4345 grains;

13%), the noctuid moth Bulia deducta (2130
grains; 0%), the bee Sphecodogastra noctivaga

(1755 grains; 5%), and the introduced honey bee
Apis mellifera (1500 grains; 5%). So although noc-
tuid moths 1 'ctively appear to be important pol-
linators of Gaura villosa, the antlion Scotoleon and
the two species of Sphecodogastra bees are the ma-
jor pollen carriers for this species, responsible for
nearly three-quarters of the total pollen load in this
analysis.

The activity of these major pollinators spans the
entire time of day and night during which Gaura
villosa flowers were open. In the 1960s, Gregory
45 P.M.
and ceased sampling around midnight. In the
drought years of 1999 and 2000, the flowers opened
10:00 P. u. In May 2000, we clocked the
р.м. The
ers, which last only one day, then remained open

—

began collecting pollinators as early as 7:

later, after
opening of the first flowers at 10:35 flow-
for several hours after sunrise (a few as late as
10:00 A.M.).

Most of the insects collected from anthesis to
midnight were noctuid moths in the subfamily Ca-

Volume 91, Number 3

Clinebell et al. 377

Pollination Ecology

tocalinae, especially Bulia deducta and Melipotis
indomita. In the drought years, these were joined
around midnight by a variety of winged adult
lions, especially Scotoleon minusculus (of both sex-

ant-

es). but also including four other species of ant-
lions. In the non-drought year of 2001, Gaura

villosa flowers opened about 9:00 P.M., and moths
and antlions were encountered foraging together
from 9:30 P.M. until morning. Throughout the night,
onagrad oligoleges in the sweat bee family Halic-
tidae (Sphecodogastra noctivaga, both sexes) were
After
sunrise, another halictid oligolege, Sphecodogastra
danforthi, actively foraged for pollen on both the
Gaura and nearby Calylophus berlandieri. This spe-
cies was collected at Gaura flowers in both May—

also collected, mostly in sweeps for moths.

June and August-September observational periods,

and sometimes carried mixed loads of Gaura and

Sphecodogastra danforthi re-
Another hal-

Calylophus pollen.
mained active until about 9:30 A.M.
ictid bee and onagrad oligolege, Evylaeus sp. 1. was
also collected in the morning on Gaura. While this
species is not abundant in this data set, it is well
represented in another collection made at the Ki-
owa National Grassland (Union County, New Mex-
ico, U.S.A.) in July 1999 (Clinebell, unpublished
data), where Sphecodogastra danfortht was not col-
lected.

Linsley and MacSwain (1962) reported Spheco-
dogastra texana and S. noctivaga as geographical
replacements, with S. texana occurring largely te
the east of the Monahans Sandhills and S. nocti-
Those authors reported the two

raga to the west.
species as sympatric from the sandhills alone, but
all specimens in our collection key to 5. noctiraga.
Ecologically, these two species are similar and
unique within Sphecodogastra in that they are the
only known nocturnal species in the genus, which
is otherwise crepuscular or matinal; this includes
S. danforthi in our analysis.
CALYLOPHUS BERLANDIERI SPACH SUBSP. BERLANDIERI
Like Gaura villosa, this self-incompatible ona-
grad taxon has a long blooming period from March
to September throughout Texas, western Oklahoma,
and adjacent regions (Towner, 1977). Clinebell
studied this species in June and August-September
1999, May 2000, and May 2001 at the Monahans
Sandhills (site 9, Table 1). All study populations
grew intermixed with Gaura villosa. Anthesis of this

species occurs shortly before sunrise (Towner,

1977) when the halictid bee Sphecodogastra dan-
forthi begins to forage. This bee species remains

active only from sunrise until about 9:30 A.M.. but

accounts for almost half of the sample of pollinators
(Table 5). In early morning, but continuing through-
out the day, pollen-eating beetles visit the flowers:
the most common beetles are the buprestid Ach-
maeodera mixta and the chrysomelid genus Altica
Altica sp. indet.). As the day progressed, beeflies
in five genera of Bombylidae, especially Heterosty-
lum robustum and Poecilanthrax effrenus, visited
the flowers. Two large anthophorid bees, in the gen-

——.

era Centris and Diadasia, visited rarely; only a sin-
gle individual of each was collected. In early May
2001. the halictid bee Sphecodogastra danforthi
was infrequent, and the major early morning pol-
linator was the bombyliid beefly Poecilognathus
scolopax.

We recorded 252 individuals representing 27 in-
sect species visiting the flowers of Calylophus ber-
landieri, and carrying a total pollen load of 52,010
grains (Table 5). In the
eroups are as follows: Hymenoptera (7 species, 106
individuals (42%), carrying 44,240 grains (85%)):
Coleoptera (10 species, 80 individuals (32%), car-
rying 4050 grains (9%)): Diptera (5
dividuals (24%), carrying 2940 grains (6%)); and
the Lepidoptera and Neuroptera, both of negligible
importance as visitors and The halictid
bee Sphecodogastra danforthi, which is also a sig-
nificant pollen carrier of Gaura villosa (Table 4),
accounts for 4096 of the individual visits, but nearly
83% of the cumulative pollen load of Calylophus
berlandieri. Several other species of beetles, bee-

order, most important

species, 60 in-

carriers.

flies. and larger bees are significant visitors to this
plant, but none of them carry more than 5% of the
total pollen load recorded. Because of the slight
herkogamy of the flowers of this species, virtually
all floral visitors are true pollinators, regardless of
whether they are visiting the flowers for pollen, for
nectar, or for both. Seasonal variation in the polli-
nator guild appears minimal in our data set. Town-
ers (1977) list of floral visitors in Potter Co., Texas,
is a qualitative subset of our collection.

GAURA COCCINEA PURSH

Both
compatible species in both the Monahans Sandhills

Gregory and Clinebell studied this self-in-

sites 4 and 8 and sites 5 and 9, respectively) and

—

in mesquite savanna (sites 1 and 6 and site 2, re-
spectively) in Transpecos Texas (Table 1). In 1964
and 1959, Gregory commenced collecting moths at
about 7:00 P.M., whereas in the drought year of
2000 the flowers opened later, between 9:00 and
9:30 р.м. This pattern of delayed anthesis is similar
to the pattern reported above for Gaura villosa in
the drought years of 1999 and 2000. At sites 5 and

378

Annals of the

Missouri Botanical Garden

Table 4.

es 4, 7);

966 (site 3); 7-12 June,

b = Mentzelia strictissima; с = Calylophus berlandieri; d = Asclepias sp. pollinia.

30 Aug.-1 S

Floral foragers on Gaura villosa subsp. е in the Permian Basin (Texas, U.S.A.: see e Table | for site
data); pooled data from 1-2 June 1964 (sit 8 June 1

ay 2000, and 6-13 May 2001 (site 9). Legend: F = ed M = male; W = worker; a

99, 20—29

- ма. Ри

Il to 51 to to

ltol0 50 100 f Other
Gaura Gaura Gaura Gaura ым Gaura pollen
pollen grains grains grains grains grains carried Totals
Coleoptera
Cantharidae
Chauliognathus sp. 1 1
Chrysomelidae
Altica sp. indet. 1 7 l 8
Diabrotica undecimpunctata Mann. l l
Diptera
Bombyliidae
Poecilanthrax effrenus (Coquillett); M 1 l
Tachinidae sp. indet. 1 l l
Hymenoptera
Andrenidae
Perdita sp. indet 1; F | l
Apidae
Apis Dea L. W 3 3
Halictidae
pee angelicus Cockerell; F | l
Agapostemon splendens (Lepel.); F l 1
Evylaeus sp. 1; Е 1 1 l 2 a(l), b(1) 5
Evylaeus sp. 1; M 3 3
Sphecodogastra noctivaga (Linsley &

MacSwain); F 13 l 5 2 2 23
Sphecodogastra noctivaga (Linsley &

MacSwain); M 1 4
Sphecodogastra danforthi McGinley; F 5 2 2 І 1 б b(1). c(1) 20
Sphecodogastra danforthi McGinley; M 6 l 7

Lepidoptera
Butterflies
Pieridae
Nathalis iole; M 2 2
Moths
Arctiidae sp. indet. 1 1 l
Geometridae
Semiothisa punctilineata (Packard) 1 1
Geometrid sp. indet. 1 l l 2
Noctuidae
Acontiinae
Acontia aprica (Hubner) 2 2
Amphipyrinae
Cosmia calami (Harvey) l l
Catoc:

Bulia pom ta (Morr.) 55 54 37 6 1 d(3) 253
Caenurgina erechtea (С ram.) l l
Melipotis indomita 24 12 4 4 2 46
Melipotis jucunda Hubner 2 l 3
Syneda howlandi Grote; M l 1

Hadenina

Pseudaletia unipunctata (Haw.)

Volume 91, Number 3

Clinebell et al.

Pollination Ecology

379

Continued.

Table 4.

ll to 51 to
50 100

Gaura Саига

No. | to

(
Gaura Gaura

101 to
500
Gaura

Other
pollen

>500
Gaura
i carried

Totals

pollen grains

grains

grains grains grains

Heliothinae
Helicoverpa zea (Boddie)
Schinia FON (J. E. Smith); V
Noctt
pum malefida Guenee
Feltia volubilis Harvey
Plusiinae
Trichoplusia ni (Hbn.)
noctuid sp. indet. 1 (small. white)
noctuid sp. indet. (12 mm, mottled brown)
noctuid sp. indet. (15 mm, mottled brown)
noctuid sp. indet. (12 mm, light tan
Pyralidae
Achyra rantalis (Guenee)
Nomophila nearctica Monroe
Sphingidae
Hyles lineata L.
moth sp. indet. (light brown)
moth sp. indet. (small, cream
moth sp. indet. (small, tan)
Neuroptera
Chrysopidae
lacewing B4 indet. 1
My cie tidae
3rac 1 5
Pin hynemurus hubbardi;
Paranthaclisis hageni; F
Paranthaclisis hageni; M
Scotoleon minusculus N. Banks: F
Scotoleon minusculus N. Banks; M
Vella fallax; M (60 mm)
1; M (40 mm)

N —

BJ ja x D$ e

antlion sp. indet.
202 101

Totals

— NN — — N л

M

20 У = 5

9, Clinebell collected early morning bees on this
species that are similar at least at the family level
to those collected in the llanos of San Luis Potosí,
Mexico, by Breedlove (collections at the Missouri
Botanical Garden, analyzed by Clinebell), and dis-
similar to morning bees collected on G. villosa and
Calylophus berlandieri as discussed previously.
The 238 individuals collected on Gaura coccinea
represent 34 species of insects (Table 6), and they
wry a cumulative pollen load of 4945 grains. Al-
though Coleoptera, Diptera, and Hymenoptera were
present, all were negligible in importance com-
pared with the Lepidoptera, especially geometrid
and noctuid moths, which account cumulatively for
86% of the individual visits and 99% of the gross

pollen load. The noctuid moth Bulta deducta was
marginally the most important species in terms of

57 and pollen carried (830

individuals (57.
grains, 17%), but at least four other moth species
Melipotis indomita, M. jucunda, Discestra trifolii,
and an undetermined species) carried nearly as
much pollen (Table 6).

The noctuid moths Bulia deducta and Melipotis
indomita are major floral visitors to both Gaura coc-
cinea and G. villosa, but G. coccinea also attracts a
wider array of other small noctuids and geometers
in the first two hours after anthesis (Table 6). We
have not yet studied Gaura coccinea between mid-
night and sunrise, so we do not know if antlions
play a role in its pollination. A number of bees that

p

—

380 Annals

of the
Missouri Botanical Garden

Table 5. Floral foragers on Calylophus berlandieri subsp. berlandierei in the Monahans Sandhills (Texas, U.S

LAS

site 9, Table 1); pooled data from 7-12 June, 30 Aug.—1 Sep. 1999, 20-29 May 2000, and 6-13 May 2001. Legend:
= female; M = male; a = Thelesperma megapotamicum; b = Mentzelia strictissima; с = Mimosa ану var.
5 d = Gaura villosa; е = Argemone polyanthemos. Counts designated with an asterisk (*) are from slides

made to quantify proportions of mixed loads of Calylophus and Gaura pollen. Specimens often edd much larger
loads (> 1000 grains) of Calylophus pollen.

lto II to 51 to LOL to
No 10 50 100 500 S500 Other
Caly. Caly. Caly. Caly. Caly. pollens
pollen grains grains grains grains grains carried Totals

5
Buprest
harder mixta 6 l 4
Cantha
Chanliognathus sp. indet. l
Chrysome lida
Altica sp

N

a(2) 13

inc t l. 15 12 16 1 3 b(2) 50
Cleridae
Trichodes oresterus Wolcott | l
Coccinellidae
lady beetle sp. indet. 1 l l
Meloidae
jM E viridis (Horn) 2 l l 4
Scarabaeidae
Ans sp. indet. l
ah ai sp. indet 1 (black and yellow) l
beetle sp. indet. 1 (black, 4 mm) 2 4
beetle sp. ada 2 (orange-brown, 5 mm) |
Diptera
Bombyliidac
nastoec А sp ; М l
Exoprosopa sp. indet. 3
od Cd la (Osten Sacken); F 3 1 5
Poecilanthrax effrenus (Coq. 10 9 a(8) 25
Poecilognathus scolopax (Osten Sacken) 4 5 6 0 |

—
С^

Hymenoptera
Anthophoridae
Centris caesalpiniae Clell.;
Diadasia rinconis; M l
pidae
PRR pennsylvanicus (DeGeer); W l e(l) 1
Halicti
yla sp. indet. l
Sphec Mei ba danforthi McGinley; F l 4 10* 80*
Sphecodogastra danforthi McGinley; M 2 2
Sphecodogastra lusoria (Cresson); F 2 2
Tiphiidae
Tiphia sp. indet. 1; F l
ne e
Danaidae
Danaus gipa (Cramer); F l e(l) l
Hesperiidae
Le € nita (W. H. Edwards) l 1
Lycaenidae
lyc acid sp. indet | l l
Noc ч
Plus
Autographa biloba (Stephens) l l
Pieridae
Nathalis iole; M l
Neuroptera
Myrmeleontidae
Scotoleon minusculus N. Banks; F |

l'otals 45 37 45 17 24 84 УУ = 252

Volume 91, Number 3
2004

Clinebell et al. 381

Pollination Ecology

are otherwise rare in our data set visit this species
in the early morning, but most of these bees, in-
cluding the anthophorid Martinapis enteicornis
(both sexes) and the halictid Agapostemon angeli-

эма,

cus (males only), carry little or no pollen. Consid-
ering the relatively high number of insect visitors
to this species, the total pollen load identified is
considerably smaller than those for other species of
Onagraceae in this analysis. It is unclear if we have
missed one or more major pollen carriers, or if this
species relies more heavily on insect visitors like
noctuid moths or small bees that individually carry
small pollen loads but that are present in large

numbers.

CALYLOPHUS HARTWEGH (BENTH.) P. H. RAVEN SUBSP.
FILIFOLIUS (EASTW.) TOWNER & P. H. RAVEN

Just as we often encountered Calylophus berlan-
«егі and Gaura villosa together on the sandiest
sites, we also noted an association between C. hart-
wegii and G. coccinea on firmer substrates. Gregory
studied the self-incompatible C. hartwegii at site 8
in the Monahans area: Clinebell studied it at both
Monahans (site 9) and in the Transpecos area (site

2). This species seems to be particularly negatively
impacted by drought; at site 9 it bloomed abun-
dantly in 2001, but was not even observed in the
drought years of 1999 and 2000. At site 2 in the
drought year of 2000, but the first
flowers did not open until 8:00 P.M., at least a half

it did bloom.

an hour rend than the same plants in the mesic
vear of 2001.

ч each evening of observation, anthesis in
Calylophus hartwegii set off a “rush” of activity by
sphinx moths. The first sphingid moths (Hyles li-
пеша) appeared at 8:15 P. M., and the last at 9:20
Р.М.
lia and Melipotis here, but they were notably less

We also collected the large noctuid moths Bu-

abundant on Calylophus than on Gaura at the same
sites. At site 2, about a third of the 54 floral visitors
were worker honeybees (Apis mellifera), which were
otherwise uncommon in the data set. By compari-
son, honeybees (and noctuid moths) did not visit
this taxon at Monahans (site 9). This underscores a
great problem for students of southwestern polli-
nation biology: where feral honeybees are abun-
dant, their presence may affect adversely the activ-
ities of native insects (Primack & Silander, 1975).
The presence of honeybees may be less of a prob-
lem in the case of sphingid moth-pollinated species
like Calylophus hartwegii, where honeybees and
sphingid moths co-forage in apparent harmony, pos-
sibly by partitioning nectar versus pollen resources.
However, in the case of diurnal bee-pollinated taxa

like C. 1977),

presence of honeybees negatively impacts the na-

berlandieri or C. tubicula (Towner,
tive bees. At a population of C. tubicula in Brewster
County, Texas, near Big Bend National Park, hon-
eybees were the major visitor and pollen carrier,
competitively excluding the native bees that are
present and presumably are the original pollinators
(Clinebell,
1977). We Po the lack of noctuid moth visi-

unpublished data; see also Towner,
tation on C. hartwegii at Monahans to the abun-
dance at the site of Gaura villosa, a preferred noc-
tuid nectar resource. By contrast, at the Brewster
County site, there were few G. coccinea plants ver-
sus many C. hartwegii plants, rendering any re-
source partitioning between the noctuid and sphin-
gid moths bioenergetically untenable.

As summarized in Table 7, 77 individuals rep-
resenting 13 species were captured on Calylophus
hartwegii, carrying a total of 11,665 pollen grains.
Lepidoptera account for most of the individuals re-
corded (50, 65%), compared to Hymenoptera (23,
30%), with Coleoptera and Neuroptera present, but
of negligible significance. However, Hymenoptera
carry a majority of the pollen load (7530 grains,
05%).
33%).
visitor (27
30%),
carries less pollen than the introduced honeybee
. 2396; with 5500 grains, 47%), which oc-

The next most abundant visitors

compared to Lepidoptera (4130 grains.
The sphingid moth Hyles is the most common
35%; 3535

especially at Monahans (site 9), but overall

individuals, with grains,

Apis (18
curs only at site 2.
are noctuid moths Bulia (7 individuals, 9%) and
Melipotis (5, 6%) and the native halictid bee Sphe-
codogastra danforthi (5, 6%), but in terms of pollen
loads, the latter carries significantly more pollen
(2030 grains, 17%) than the noctuids (both 140
grains, 1%). In fact, the single individual of the
arge sphingid moth (Manduca quinquemaculata)
encountered carried more pollen (ЗОО grains, 3%)

than all of the noctuid moths combined. It appears
that all of the Hymenoptera reported on C. hartwe-
gii are pollen robbers rather than pollinators, as
they do not contact the stigmas during their forag-
ing, whereas the sphingid moths always made con-
tact. Similarly, the noctuids also appear to be large-
ly nectar robbers. Thus, only the sphingid moths
were effective pollinators, due to the extreme her-
kogamy of the flowers.

Most of the pollen of Calylophus hartwegii, a
self-incompatible species, was moved by sphingid
Monahans, and at other

—

moths (Hyles lineata) a
sites by sphingids and honeybees, with smaller
amounts of pollen carried by the noctuid moths Bu-
lia deducta and Melipotis indomita (Table 7). Greg-
ory (1964) also studied this taxon (as Oenothera

382

Annals of the
Missouri Botanical Garden

Table 6.
7 and 16 May 1959 (sit
= Mimosa quadrivalvis var. mala c

Floral vigi on Gaura coccinea from sites in
1-2 June 1964 (sites 1,
= Asclepias sp. pollinia.

4, 8):

Texas, U.S.A. (see Table 1 for site data); pooled data from

and 22-28 May 2000 (site 9). Legend: a =

Dalea sp.; b

1 51 to 101 to

l
50 100

—
=
o

No | to 500 2500 Other
aura Gaura Gaura ura Gaura Gaura pollens
pollen pollen pollen pollen pollen pollen carried Totals
Coleoptera
Buprestidae
Achmaeodera mixta 1 а 1
Chrysomelidae
ltica sp. indet. 1 7 1 11
Cleridae
Trichodes oresteres Wolcott l 1
Diptera
Bombyliidae
Poecilognathus scolopax (Osten Sacken) 4 4
Hymenoptera
Anthophoridae
Martinapis enteicornis (Clell.); F l l
a enteicornis (Clell.); M 2 3 l a(5), b(1) 6
Halictidae
3 angelicus Cockerell: M 7 3 10
Lepidoptera
oths
Geometridae
'emiothisa sp. indet. | (small, tan) 14 19 9 5 47
Se otogramma ae p Smith l l
geometrid sp. indet. | (18 mm, brown) 1 l l 3
Noctuidae
Acontiinae
Acontia кы (Hubner) 1 1
Acontia sp. indet. 1 (5 mm, brown) 6 1 7
Acontia sp. йй. 2 (8 mm, black 2 2
& tan)
Cobubatha orthozona (Hampton) l l
Catocalinae
Bulia deducta (Morr.) 29 13 13 1 1 c(2) 57
Matigramma rubrosuffusa Grote 2 2
Melipotis indomita Wk. 3 16 3 22
Melipotis jucunda Hubner l l 6 1 9
Hadeninae
Discestra ipu Low D 1 1
Leucania sp. indet 1 l 2
hadeninid sp. ine. P 5 mm, with l l
brown reticulations)
Heliothinae
Helicoverpa zea (Boddie) 2 4 4 2 12
5с hinia citrinella l l 2
Nocti
de пай Guenee l l
noctuinid sp. indet. | l 1
Plusiinae
Ra pum ou (Guenee) l 1
moth sp. indet. 1 (small, tan) | 1 2
moth sp. seid 2 (small, brown) l 1
7 1 2 l 2 16

moth sp. indet. 3 (small, tan with brown і
markings

Volume 91, Number 3

Clinebell et al. 383

Pollination Ecology

Table 6. Continued.
Il to 51 to 101 to
No ‹ 50 100 500 2500 Other
Gaura Gaura Gaura Gaura Gaura Gaura pollens
pollen pollen pollen pollen pollen pollen carried Totals
moth sp. indet. 4 (13 mm, dark brown) | | 2
Pyralidae
Pyraustinae
Pyraustinae sp. indet. | |
Diatsictis fracturalis is 3 3
Epipagis huronalis (Guenee) 2 | | |
pyralid sp. indet. 1 (13 mm, reddish) | |
Sphingidae
Hyles lineata L. l |
Totals 94 64 60 15 4 | УУ = 238
hartwegii) in the Monahans area. He described vis- abundantly. In the course of several hours of ob-

itation by large bees in Melissodes (Anthophoridae)
and Megachile (Megachilidae) in the hour before
sunset, and anecdotally ascribed to bees the ma-
jority of the pollen transfer. We did not observe
these bees visiting C. hartwegii in our studies in
Instead, we found these

the same general region.

—

large bees on Argemone polyanthemos (Table 10).
and in no cases did they carry any onagrad pollen.
We include here observations of two additional
species of Onagraceae tribe Onagreae that occurred
sporadically at the Monahans site 9 (Table 1). How-
ever, these species were not present in sufficient
numbers to allow us to analyze their pollination bi-
ology completely.
OENOTHERA RHOMBIPETALA NUTT. EX TORR. &
A. GRAY

Clinebell studied this species in June 1999 at
Monahans (site 9) with Calylophus berlandieri and
Gaura villosa on stabilized dunes, but blooming
plants were absent in the severe drought year 2000.
During a fairly short observational period of six
hours (Table 2) in 1999, he collected three sphingid
moths (Hyles lineata), three noctuid moths (Meli-
potis indomita), and a beetle (Eupompha viridis
Horn). This anecdotal information suggests that 0.
rhombipetala, with long corolla tubes (2.5-3 cm
long), is pollinated primarily by sphingid moths,
much like C. hartwegii, which also possesses long

corolla tubes.

OENOTHERA ENGELMANNII (SM ALL) MUNZ

Clinebell observed this species at Monahans in
1999 and 2000, but the plants were never in bloom.

In May 2001,

however, O. engelmannii bloomed

servation in early morning and early evening, few

insects visited its flowers. Additional fieldwork
needed for this species.

In addition to the six onagrads just discussed,
Clinebell collected floral visitors on three taxa that
bloomed at the same time in these communities:
Thelesperma megapotamicum (Asteraceae), Mentze-
lia strictissima (Loasaceae), and Argemone polyan-
1). We include them

in the analysis as part of a community-ecology ap-

themos (Papaveraceae; Table 1

proach to the study of Onagraceae pollination, in
order to identify flower-visiting insects shared with
the onagrad taxa as well as those that do not come
to the onagrads. These three non-onagrad species
co-occurred with Calylophus berlandieri and Gaura
villosa in the stabilized dune areas of site 9 (Table
l; Fig
THELESPERMA MEGAPOTAMICUM (SPRENG.) KUNTZE
Commonly known as Navajo tea, this species of
Asteraceae was abundant in the stabilized dunes and
attracted numerous beeflies and scoliid wasps. A to-
tal of 56 insects in 22 species carried a cumulative
load of 10,950 pollen grains (Table 8). The colorful
orange and black beefly Poecilanthrax effrenus was
the most common visitor (15 individuals, 27%) and
carried much of the pollen moved (3390 grains,
31%).
tea and the onagrad Calylophus berlandiert. The sin-
ele individual encountered of the large beefly, An-

This beefly divided its time between Navajo

thrax sp. indet. (at 15 mm long, as large as a small
bumblebee), also carried a large load of Thelesperma
The next most abundant pollen carrier was
another beefly, Exoprosopa sp. | (11 individuals,

20%), which carried 760 pollen grains (7%). The

pollen.

384 Annals of the
Missouri Botanical Garden
Table 7. Floral foragers on Calylophus hartwegii subsp. filifolius in the Permian Basin and Transpecos region (Texas,
.S. A.: see Table | for site ч, рв data from 2 June 1964 (site 8); 22-28 May 2000 (site 2); and 6-13 Мау
2001 (site 9). Legend: F = female male; M = worker; a = Dalea sp.: b = Gaura villosa; с = Solanaceae or
Nyctaginaceae; asterisks (*) refer to MS records, pollen load unknown.
11 to 51 to 101 t
No | to 10 50 100 500 500 Other
Caly. Caly. Caly. Caly. Caly. Caly pollens
polle n grains grains grains grains grains carried Totals
Coleoptera
Chrysomelidae
Altica sp. indet. 1 2 l 3
Hymenoptera
Apidae
cl ш I. W 7* 11 a(2), b(1) 18
Halic
ra NN danforthi McGinley; F l 4 5
Lepidoptera
Moths
Noctuidae
Acontiinae
acontiinid sp. indet. 1 (brown, 7 mm) 3 3
Catocalina
Bulia didus ta (Morr.) 3 l 2 l 7
Drasteria pallescens (Grote & Robin- l |
son)
Matigramma rubrosuffosa Grote | |
Melipotis indomita МІК. 1 | 2 l 5
Heliothinae
Shinia citrinella (Grote & Robinson) 3 І 4
“с
astictis киши: (Zeller) 1 |
Sphing aT
Hyles li "d 11. 7* 2 5 5 5 3 c(l) 27
Manduca quinquemaculata (Haworth) | с l
Neuroptera
Myrmeleontidae
Scotoleon minusculus (N. Banks); M 1 1
Totals 28 8 10 7 6 18 У = 77

third most common pollen carrier, which was еп-
countered nowhere else in this data set,
small orange-yellow scoliid wasp Trielis octomacu-
lata (4 individuals, 7%), carrying the second largest
amount of pollen (2000 grains, 18%). Two individ-

undetermined wasp carried the third we
est шош pollen load (1000 grains, 9%).
least 11 different insect species carried significant
loads of Thelesperma pollen (> 100 grains), many of
them represented in the data set by only a single
specimen (such as the beefly Anthrax).

was the

MENTZELIA STRICTISSIMA (WOOTON & STANDL.) J. DARL.
A sample of 42 floral visitors in 11 species, car-
rying a cumulative pollen load of 16,790 grains and

collected at site 9 in June and Aug.—Sep. 1999 (Ta-
ble 1), shows no significant overlaps between this
species of Loasaceae and any co-blooming ona-
grads (Table 9). Bees accounted for most of the vis-
itors (35 individuals, 83%) and carried most of the
pollen (16,025 grains, 95%); only one beefly (Dip-
tera; 2% pollen carried), one skipper (Hesperiidae;
Lepidoptera), and five beetles (Coleoptera; 2% pol-
len carried) were collected on Mentzelia. The co-
dominant visitors to M. strictissima are worker bum-
blebees (Bombus pennsylvanicus) and females of the
green halictid bee Agapostemon splendens, each
with 10 individuals (24%) that carry cumulatively
5000 grains (30%) each. Both species are rare else-

—

Volume 91, Number 3 Clinebell et al. 385
2004 Pollination Ecology

кеч 8. Floral foragers оп Thelesperma megapotamicum (Asteraceae) in the Monahans sandhills (Texas. U.S.A.:
site 9, Table 1): pooled data from 7-12 June, 30 Aug.-1 Sep. 1999, 28 Мау 2000, and 6 May 2001. Legend: F =

fe ко М = male: a = Mimosa quadrivalvis var. occidentalis: b = Argemone ا‎ c = Calylophus berlandieri.

11 to 51 to LOL to
No J to 10 50 100 500 S500 Other
Thele. Thele. Thiele. Thiele. Thiele. Thiele. polle ns

pollen grains grains grains grains grains carried Totals
Coleoptera
Cleridae
Thrichodes oresterus Wolcott | 1
Chrysomelidae
Diabrotica undecimpunctata Mann. 1 l
coleopteran sp. indet. 1 (gray) l l
Diptera
Bombyliidae
Anthrax sp indet. 1 l
Chrysanthrax s (Sav) | | 2
Exoprosopa sp. indet. l 5 2 | 2 11
Exoprosopa sp. indet. 2 | |
Poecilanthrax effrenus (Coquillett): M 1 2 1 |
Poecilanthrax effrenus (Coquillett): F l |
Poecilanthrax effrenus (Coquillett); М+К 3 3 2 2 10
Bombyliid sp. indet. l l
Syrphidae
Eristalis sp. indet. 1 1 1
Tachinidae sp. indet. 1 | 2 3
Hymenoptera
Halictidae
Agapostemon angelicus Cockerell; M 2 2
Sphecodogastra danforthi McGinley: К 1 l
lehneumonidae
ichneumonid sp. indet. ! | |
Scoliidae
Trielis octomaculata texensis (S. SS.): M 1 |
Trielis octomaculata texensis (S. ss.); F З a(2). bel) 3
Sphecidae
Sphex sp. indet. 1; F 1 1
Vespidae
Eumeninae sp. indet. 1; M 1 l
wasp sp. indet. 1; M 2 a(l) 2
Lepidoptera
Lycaenidae
lycaenid sp. indet. 1 (small, blue) | 1
Nymphalidae
Euptoieta claudia (Cramer) 2 1 e(l) 2
Pieridae
Colias philodice philodice Godart; l 1
Nathalis tole Bois.: F 1 l
Totals | 10 10 8 10 14. 22, = 56

where in our data sels. Perdita kiowi. a small ARGEMONE POLYANTHEMOS (FEDDE) С. B. OWNBEY
cream-colored andrenid bee that is active at twi-

light and well-camouflaged on the Mentzelia This species intergrades considerably with Ar-
blooms. is found nowhere else in our collections. gemone albiflora Hornem. subsp. texana С. B.

386 Annals of the
Missouri Botanical Garden
Table 9. Floral foragers on Mentzelia strictissima (Loasaceae) in the Monahans sandhills (Texas, U.S.A.: site 9,

Table 1); pooled data from 7-12 June 1999 and 30 Aug.-1 Sep. 1999. Legend: F =

a — Argemone polyanthemos.

female; M —

male; W — worker;

| to j^ to 51 to 1011
100 500 >500 Other
. Ment. Ment Ment. Ment. Ment. pollens
MM n grains grains grains grains grains carried Totals
Coleoptera
coleopteran sp. indet. 1 (11 mm, gray) 3 | 5
Diptera
Bombyliidae
Poec ilognathus scopulax (Osten Sacken); F l l
Hymenoptera
Andrenidae
Perdita kiowi Griswold; M 2 2
Perdita kiowi Griswold; F 1 l 2
Apidae
Apis mellifera L.; W 1 1
Bombus HM anicus (DeGeer); W 10 a(2) 10
Halict
о angelicus Cockerell; F | l
Agapostemon splendens (Lepel.); F 10 10
Agapostemon splendens (Lepel.); M 3 3
Augoc UE sumptuosa (Smith); Ё l a(l) l
Dialictus sp. indet. 1; F l l
Evylaeus sp. na I: F l l
Lepidoptera
Hesperiidae
Atalopedes campestris huron W. H. Edwards; M l 1
Totals 3 4 3 3l 2 = 42
Ownbey (Papaveraceae) in central Texas, and al- vaga) carrying significant pollen loads (= 300
though the two are considered to be distinct spe- grains each) also were unique in the data set, as

cies, these white prickly poppies are often not eas-
ily separable (Diggs et al., 1999). We have treated
the specimens from the Monahans Sandhills (site
9) as A. polyanthemos. Most of the 72 floral visitors
n this sample, belonging to 18 species and cu-

mulatively carrying 27,140 pollen grains (Table
10), show no overlap with the insects sampled on
Onagraceae. Hymenoptera account for most visitors
(56, 78%) and most pollen carried (23,895 grains,
88%), with Coleoptera (10, 14%; 2405 grains, 9%)
and Diptera (5, 7%; 930 grains, 3%) also present.
Females of the anthophorid bee Diadasia rinconis
are unique to Argemone in the data set, though one
also carried some Mentzelia pollen. Both males (20
individuals, 2896) and females (11, 1596) of this

‘actus bee were the most common Argemone pollen

carriers; altogether, Diadasia rinconis carried
13,100 grains (48%). One male and two female
long-tongued megachilid bees (Megachile monti-

were two other species of Megachile. The halictid
bee Augochloropsis sumptuosa was otherwise found
only on Mentzelia. We collected four individuals

6%) of Evylaeus sp. 1, another halictid bee com-

—

monly encountered on species of Onagraceae; no-
tably, one of the specimens captured on Argemone
had a pollen load with 90% Gaura pollen. The an-
thophorid and megachilid bees were mostly col-
lected in early morning, sleeping in the flowers in
the crevice between the stamen cluster and the pet-
als, often in groups. Since the stigma of this species
is located at the center of the ball of stamens, these
bees would have to crawl to the top of the stamen
ball before flying off in order to effect pollination,
and this was not observed. However, this spatial
arrangement of stigma and stamens applies to all
floral visitors, and we have no observations that
would single out one group of visitors as being more
or less effective as pollinators.

Clinebell et

Volume 91, Number 3 al.
4 Pollination Ecology

Table 10. Floral foragers on Argemone polyanthemos (Papaveraceae) in the не Sandhills (Texas, U.S.A.: site
Table 1); pooled data from 7-11 June 1999 and 6-8 May 2001. Legend: M = male; F = female: a = Onagraceae:
A = Calylophus berlandieri; с = Mentzelia strictissima: d = Gaura villosa.
lto II to 51 to 101 to
No 50 100 500 500 Other
Arge. Arge Arge. Arge. Arge. Arge. pollens
pollen grains grains grains grains grains carried Totals
Coleoptera
Chrysomelidae
Altica sp. l l
Diabrotica undecimpunctata Mann. ] l
Coccinellidae
coccinellid sp. indet. 1 l a l
Meloidae
Eupompha viridis (Horn) 4 l 5
coleopteran sp. indet. 1 (red thorax) 2 2
Diptera
Bombyliidae
Poecilognathus scopulax (Osten Sacken) 1 b |
bombyliid sp. indet. 1 (tiny, wings clear) l |
Syrphidae
Eupeodes volucris Osten Sacken; F 2 2
Eupeodes volucris Osten Sacken; M l l
Hymenoptera
Anthophoridae
entris atripes Moes. ] |
Diadasia aff. diminuta (Cr.); F ] 3 1
Diadasia rinconis Clell.; t | З 7 c(1) 11
Diadasia rinconis Clell.: 5 15 20
Halictidae
5 sumptuosa (Smith); F 2 2
тец indet. l 3 c(1), d(1) 1
Spr Зани McGinley; Е | |
Megachilic
Megachile e laurita; F 1 4 5
Megachile montivaga Cresson; F 2 2
Megachile montivaga Cresson; М | |
Megachile mucurosa Clell.: l l
Megachile mucurosa Clell.; 3 2 2 |
Lepidoptera
Noctuidae
Plusiinae
Autographa biloba (Stephens) 1 1
Totals 4 3 2 23 40 У = 72

SUMMARY OF MAJOR POLLEN CARRIERS

For this analysis, we define major pollen carriers
as insects carrying more than 50 pollen grains of a
given plant species; Table 11 lists those major car-
riers for each of the seven plant species for which
Table 12

pools major pollen carriers by plant species and

we have enough data. For convenience,

shows that there is great specificity in each pollen
guild. What is remarkable about these tables is the

significant absence of overlap among the major pol-
len carriers in terms of the plant species they visit.
These are unexpected results that argue for the
need to conduct more field studies in pollination
biology at the community level. Although it has
been difficult to get insect determinations across
this data set and tedious to quantify the pollen
loads, we feel that these data demonstrate a higher

level of pollinator specialization in these commu-

388 Annals of the
Missouri Botanical Garden

Table 1

plant species. Insect taxa represented in the data set by a single specimen (“singleton”) are marked with an asterisk

Major pollen carriers by plant species, defined as any insect carrying more than 50 pollen grains of that

(*) and included in the closest inclusive taxon in which they can be determined.

Thele-

sperma Mentzelia Argemone
Gaura Calylophus Gaura Calylophus mesopo- stric- oly-
villosa berlandieri coccinea hartwegii tamicum tissima anthemos

Coleoptera 17
Buprestidae
Achmaeodera mixta і
Jeridae 17
Chrysomelidae
Altica sp. indet. | l
Meloidae
Eupompha viridis 5
Scarabaeidae
Coleoptera sp. indet. | 2
Diptera
Bombyliidae 3*
Exoprosopa sp. indet. | 3
Heterostylum robustum 6
Poecilanthrax effrenus 12
Poec Т scopulax 7 l l
Syrphidae
Бонн volucris 2
Tachinidae indet. | 3
Hymenoptera
Apidae
Apis mellifera 3 11 4
Bombus pennsylvanicus l 10

5 2*
asia aff. diminuta 4
). rinconensis 30
б. lac 1"
opem angelicus | l

>

А. splendens 13
Augochloropsis sumptuosa 1 2
Evylaeus sp. indet. 1 2 l 4
Sphecodogastra danforthi 11 94 1 1
S. noctivaga 4

Megachilidae

w

еа hile montivaga
M. тис
M. cf. ашы

© л

Scoliidae
Trielis octomaculata 4

Sphecidae | +

Vespidae l
wasp indet.

Lepidoptera

Geometridae

Semiothisa sp. indet. 5

Volume 91, Number 3 Clinebell et al. 389
Pollination Ecology

Table 11. Continued.
Thele-
sperma Mentzelia Argemone
Gaura Calylophus Gaura Calylophus mesopo- stric- oly-
villosa berlandieri coccinea hartwegii tamicum tissima — anthemos
Noctuidae 4* 5%
Bulia deducta 7 2 1
Helicoverpa zea 2
Velipotis indomita 6 3 l
noctuid sp. indet. 3 3
Рена [*
Hyles lineata 13
Neuroptera
Myrmeleontidae |*
Brachynemurus hubbardi 3
Paranthaclisis hageni 3
Scotoleon minusculus 69
Total: singletons 5 3 5 l 7 3 2
Total: all major pollen carriers 114 125 20 3l 32 38 65

nities than expected, based on current debate re- (the overall “community efficiency” is 33.3%), sug-

garding specialized versus generalized pollination gesting considerable variability among species.

niches (Waser et al.. 1996). In summarizing polli- At the other extreme, many rare insect species
nator activity (Table 13), we found that the guild also appear in this large data set. Whether it is the
arge scarab flower beetle Euphoria on Calylophus

fidelity of the seven main plant species ranges from
75.0% to 99.2%, with a mean of 91.2%. Pollen berlandieri, the large antlion Vella fellax on Gaura
transport efficiency ranged from 8.4% to 90.5% in villosa, or the large beefly Anthrax on Thelesperma

the seven taxa. with a mean of 50.9% efficiency megapotamicum, these insect rarities represent an

Table 12. Pollination guilds of major pollen carriers for each of the primary plant species in this analysis, as
detailed in Table 11. Insect taxa (including singletons) are assigned to the guild of the plant whose pollen they primarily
ie., serve as modal pollen carrier); individual insects that are major pollen carriers for other (non-modal) plant

ies. The halictid bee Agopostemon angelicus (only one individual each on Gaura villosa

—

curry
species appear under those speci
and Mentzelia strictissima) is assigned to Guild 6 (of Mentzelia) because that individual carried a larger load and Guild

6 also includes A. splendens.

Thele-
erma Mentzelia Argemone
Gaura Calylophus Gaura Calylophus megapo- stric- poly-

villosa berlandieri coccinea hartwegii tamicum tissima anthemos

Guild 1 97 5 2
(Gaura villosa)

Guild 2 11 124 | | | l
(Calylophus berlandieri)

Guild 3 15
(Gaura coccinea)

Guild 4. 3 25 4
(Calylophus hartwegii)

Guild 5 31
(Thelesperma megapotamicum)

Guild 6 | 1 31
(Mentzelia strictissima)

Guild 7 2 2 64

Argemone polyanthemos)

—

390

Annals of the
Missouri Botanical Garden

Table 13.

Community summary statistics.

The overall community pollen transport efficiency (marked *) is an

average for all insect visits observed; this figure is biased by the unequal pollinator sample sizes among the plant

species. The mean guild pollen transport efficiency (marked *

seven guilds, is not biased by unequal sample sizes.

*), the average of the efficiency figures for each of the

s modal
najor

Total non-modal Guild pollen

jor Total floral major pollen Guild ransport
їй carriers isito carrier fidelity D efficiency (96)
A C АДА + (A+C)/B
Gaura villosa 97 562 17 85.1 20.3
Calylophus berlandieri 124 252 1 99.2 49.6
aura coccinea 15 238 5 75.0 8.4
Calylophus hartwegii 25 77 6 80.6 40.3
Thelesperma incip um 31 56 l 96.9 97.1
Mentzelia strictiss 31 42 7 81.6 90.5
Argemone ш ш 64. 72 l 98.5 90.3
XX = 394 УУ = 1299 = 38 91.2 33.3*
Mean guild pollen transport efficiency: 50.9**

important secondary outcome to the randomized
field collection of a sufficiently large sample of the
common pollen carriers to enable statistical anal-
ysis of the data. These data also highlight the im-
portance of setting aside large areas of natural ref-
uges for the sake of rare species that exist at
relatively low population densities, yet play impor-
tant roles in the pollination biology and ecology of
natural communities.

DISCUSSION

We divide the discussion into two parts: (1) for-
aging behavior of major pollinating insect groups,
and comparison with other pollination studies of
Onagreae, and (2) analysis of mixed pollen loads
carried by foraging insects. Within these areas of
discussion, we examine and compare three inter-
related themes: (1) geographic replacement of re-
lated pollinators across the range of a plant species;
(2) the effect of the presence or absence of large
numbers of honeybees at a particular site; and (3)
the importance of the ecological integrity of the
community. The first two themes were highlighted
in the Results section to underscore their high im-
portance, and the third theme underpins this entire
analysis. The communities studied here represent
the most ecologically intact study areas that could
be located for these plant species, and represent
relicts of the original (i.e., pre-European settle-
ment) vegetation. Pollination studies conducted in
degraded areas may well yield different results than
those reported here.

l. FORAGING BEHAVIOR OF MAJOR POLLINATING
GROUPS

We discuss these in a diurnal sequence begin-
ning at sunrise. We note especially those cases
where a given insect is a true pollinator in one
species of onagrad, but not of other species.

Halictid bees (Hymenoptera) that are onagrad
oligoleges

At least three species of Sphecodogastra and Ev-
ylaeus visit onagrad species in the Monahans Sand-
hills. Sphecodogastra noctivaga, the largest (12 mm
long) halictid, visits only Gaura villosa, mostly from
midnight to 6 A.M., but occasionally until 8 A.M.
Both sexes of this species are unique among insect
visitors to G. villosa in that they spent the evenings
on the inflorescences, crawling about and resting.
They are highly attracted to lights, and were col-
lected by both Gregory and Clinebell at car lights
adjacent to colonies of G. villosa. Males did not
appear to carry any pollen, and females often car-
ried small pollen loads; however, females occasion-
ally carried large amounts of pollen in a full rear
femoral scopal load for the provisioning of young.
The efficacy of S. noctivaga as a pollinator is not
known because we were unable to observe their
behavior on flowers due to darkness. All bees col-
lected of this species carry only Gaura villosa pol-
en.

We collected Sphecodogastra danforthi on Gaura
villosa and Calylophus berlandieri (both Onagra-
ceae). These halictid bees forage on G. villosa,
where they were found almost exclusively in the

Volume 91, Number 3
2004

Clinebell et al.
Pollination Ecology

morning, from sunrise until about 9:30 A.M. Sphe-
codogastra danforthi was also infrequently captured
at dusk on both species of Calylophus. This species
is much more prevalent on C. berlandieri, account-
ing for about 40% of individuals (and 83% of pol-
len carried) of the pollinator data set for that spe-
cies, than on Gaura,
5% of visitors (and 13% of pollen carried).
halictid bee is an effective pollinator of Cal ylophus

where it accounts for about
This
berlandieri, frequently climbing over the stigma
while traveling from stamen to stamen. It appears
to be less effective on Gaura villosa, however, due
to the more pronounced herkogamy in the latter
species, where the stamens (6.5-13.5 mm and clus-
tered in the lower quarter of the zygomorphic flow-
er) are notably separated from the stigma (atop the
style 10-18.5 mm; Raven & Gregory, 1972a). Nev-
ertheless. we observed females using the stigma as
a landing platform several times, and so pollination
might be effected occasionally. Of 135 individuals
of Sphecodogastra danforthi in the overall data set.
18 carried no onagrad pollen, but only 2 were cap-
tured on non-onagrad taxa, | each on Argemone and
Thelesperma, carrying pollen of those species. Four-
teen individuals carried mixed loads of Calylophus
and Gaura pollen, 13 of which were captured on
Calylophus flowers. Thus, the 2 Sphecodogastra
halictid bees, 1 nocturnal and 1 matinal,
overwhelming preference for foraging on species of

exhibit an

Onagraceae.

Evylaeus sp. 1 is not as common in the data set
as Sphecodogastra, but females do carry onagrad
pollen loads. Evylaeus lacks the hooked scopal
hairs of Sphecodogastra (a synapomorphy for the
genus; McGinley, 2003) that presumably. provide
better pollen adherence for that genus. Most of the
specimens were captured on Gaura villosa from
0:30 to 8:30 A.M.,
dogastra danforthi. It is doubtful that Evylaeus is a

and these foraged with Spheco-

reliable pollinator for G. villosa for the same rea-
sons stated above for Sphecodogastra. Of 13 indi-
viduals collected in this study, 4 were found on
Argemone, and so this halictid bee is not as closely
associated with Onagraceae as are the 2 species of
Sphecodogastra.

To summarize, females of Sphecodogastra nocti-
vaga appear to be major effective pollinators of
Gaura villosa (pending verification by ethological
observations); Sphecodogastra danforthi is an effec-
tive pollinator of Calylophus berlandieri, but prob-
ably not of C. villosa; and Evylaeus sp. l may not
be an effective pollinator of either onagrad species
and does not even visit Calylophus flowers. Evy-
laeus is uncommon in this data set, and under-
standing its role at the Monahans Sandhills may

require an even larger sample size than reported
here, as is also the case for other rare species in
the data set.

We tested the Bs hypothesis that Sphecodogas-
tra. danforthi and S. noctivaga randomly visited
flowers of Cabylophis berlandieri and Gaura villosa
using the Chi-square test for independence (Con-
over, 1980).
were females, the test was calculated first using

While most individual floral visitors

both male and female bees. The Chi-square test
statistic was 61.31 (P « 0.01), indicating signifi-
cant non-random (selective) flower visitation. The
test statistic for females only was 60.69 (P < 0.01).
again indicating significant deviation from expec-
tation. These tests scored the bees according to the
plant species on which they were collected. Be-
cause 17 of the female Sphecodogastra danforthi
collected on Calylophus carried mixed loads of Ca-
lylophus and Gaura pollen, a test was run assigning
half of these mixed-load bees to Gaura. The re-
sulting test statistic, 46.83 (P « 0.01), was still
highly significant. While collecting efforts began at
7:00 A.M., after which time few Sphecodogastra
danforthi were collected on Gaura, there obviously
was an earlier period of activity that included floral
visitation to Gaura. Whether or not this included a
significant number of females that visited only Gau-
ra and had ceased foraging before 7:00 A.M. is un-
known. A conservative interpretation of these data
suggests that Sphecodogastra постава does not
visit Calylophus at all, that females of Sphecodo-
gastra danforthi visit both plant taxa. and that these
data may be biased in terms of under-representing
visits to Gaura by Sphecodogastra danforthi, if in-
deed these female bees are more likely to visit Gau-
ra than Calylophus prior to 7:00 А
Gregory collected most individuals of Sphecodo-
gastra noctivaga in this data set in June 1964
around the dome light of a car parked beside a
population of Gaura villosa, and most of these fe-
males carried either no Gaura pollen or sparse pol-
len loads. However, in August 2001.
30 female S. noctivaga bees on C. villosa in the

we collected
Ci imarron National Grassland (Morton Co., Kansas,

S.A.). all carrying large Gaura pollen pm (un-
8 9 These are the only active nocturnal pol-
len foragers on G. villosa at both sites. (The other
nocturnal floral visitors, noctuid moths and ant-
lions, actively harvest only nectar, but passively
transport pollen as a byproduct of nectar foraging.)
By contrast, 5. noctivaga appears from our data to
be less abundant at the Monahans Sandhills in Tex-
as, and it is likely that 5. danforthi visits both on-
agrad taxa in the presence of low densities of &.
noctivaga and for whatever reasons, visils Gaura

Annals of the
Missouri Botanical Garden

before Calylophus. Clinebell collected a large set
of male 5. noctivaga on 22 July 1999 from 1:30 to
3:30 A.M. on the Kiowa National Grassland, Union
County, New Mexico. Here, the males carried vir-
tually no pollen, and appeared to be searching for
females on Gaura inflorescences. We emphasize
that C. villosa was in bloom in this data set from
earliest May to early September, and that while the
insect groups collected at Cimarron, Kiowa, and
Monahans were the same from site to site, the rel-
ative abundances of these groups varied according
to site and season. The most dramatic seasonal shift
observed was the rarity of Sphecodogastra danforthi
in early May 2001 at Monahans on flowers of C.
berlandieri. While pollinator activity always oc-
curred in early morning, the major pollinator in the
absence of S. danforthi was the small beefly, Poe-
cilognathus scolopax.

Clearly, pollen load analysis has been essential
for elucidating the complexities of pollinator foraging
choice, especially when the pollen grains of related
onagrad genera can be distinguished (Praglowski et
al.. 1988).
concluded (erroneously) that Sphecodogastra danfor-

Without such analysis, we might have

thi does not visit flowers of Gaura и when in
fact it does, but only prior to 7:00 A

A single female of Sphec йн pa was
collected on Thelesperma and carried a full load of
its pollen. Four females of Evylaeus sp. | were col-
lected on Argemone, half of which were also car-
rying Gaura pollen. Otherwise, all pollen found on
these halictid bee genera was from Onagraceae

flowers.

Halictid bees (Hymenoptera) that are not onagrad
oligoleges

Three green halictid bee species included in this
data set were not major onagrad pollen carriers at
the Monahans Sandhills in Texas. Agapostemon
splendens (both males and females) occurred pri-
marily on Mentzelia strictissima, comprising about
one-third of the 42 insect visitors collected on that
All carried substantial loads of Mentzelia
pollen. Males of Agapostemon angelicus were com-

species.

mon on flowers of Gaura coccinea in early morning
at Monahans, but carried little or no pollen. Sin-
gleton females of A. angelicus were collected on
Gaura villosa and Mentzelia strictissima, each car-
rying large pollen loads, and two were collected on
Thelesperma megapotanicum, but carried less than
ten pollen grains. Thus, we do not yet know what
the females of this species are doing at Monahans.
Finally, three females of Augochloropsis sumptuosa
were collected with heavy pollen loads, two on Ar-

gemone polyanthemos and one on Mentzelia strictis-
sima. All of these bees were collected between sun-
rise and 10:00 A.M.

Other bees and wasps (Hymenoptera)

We collected bees in a diversity of families, in-
cluding Andrenidae, Anthophoridae, Apidae, and
Megachilidae, most often on plants other than On-
agraceae. Martinapis enteicornis (family Anthophor-
idae) was collected exclusively on Gaura coccinea,
but carried little pollen (Table 6). A single Diadasia
rinconis (Anthophoridae) male carried Calylophus
berlandieri pollen (Table 5), whereas 11 females
and 20 males were collected on Argemone polyan-
themos, all but one female laden with pollen (Table
10). These female D. rinconis were observed to be
sleeping inside the poppies shortly after sunrise. A
single female of Centris caesalpiniae (Anthophori-
dae) was collected on Calylophus berlandieri, car-
rying a heavy load of pollen (Table 5). A single
Bombus pennsylvanicus (Apidae) worker was col-
lected on C. berlandieri (Table 5), but ten were en-
countered on Mentzelia strictissima (Table 9), all
carrying large pollen loads of the plants visited, and
mostly collected between sunrise and 10:00 A.M.
All are putatively reliable pollinators of the plants
visited, though their densities are low in this eco-
system. Apis mellifera (Apidae) was a common pol-
len forager on Calylophus hartwegii for several
hours after anthesis at a degraded site in Brewster
County (site 2), but not at Monahans Sandhills (site
9), and the honeybee workers were not observed to
make contact with the stigmas while collecting pol-
len. They were not observed attempting to collect
nectar, which normally is quickly harvested. by
sphinx moths (Hyles lineata) that appear just at the
time of anthesis.

Five species of wasps, each in a different family
(Ichneumonidae, Scoliidae, Sphecidae, Tiphiidae,
and Vespidae) were collected on Thelasperma me-
gapotamic um at the Monahans Sandhills (site 9) in
western Texas. Almost all of these wasps (8 out of
9) carried major pollen loads (> 50 grains), so in-
dividually all except the undetermined ichneumon-
id wasp appear to be effective pollinators, albeit at
low densities in the population.

Beeflies ( Diptera)

Ten species of Bombyliidae were flower visitors
at our study sites, belonging to at least six genera.
Many beeflies visit Calylophus berlandieri, mostly
carrying small to moderate (— 100 grains) pollen
loads (Table 5); many of the numerous beeflies on
Thelesperma carry somewhat larger pollen loads

Volume 91, Number 3
2004

Clinebell et al. 393

Pollination Ecology

(Table 8). These two plant species account for most
beefly visitation in our analysis, but all plant spe-
cies except Calylophus hartwegii had at least one
beefly visitor. Beeflies tend to be most active in the
hot midday period and are very hard to catch, even
with a running start with the sweep net. We unin-
tentionally baited individuals of Poecilanthrax ef-
frenus at two separate populations of Calylophus
berlandieri at site 9 (Table 1). Although the beeflies
apparently were attracted to onagrad floral chemi-
cals on clothing and nets, we assigned them to ei-
Thelesperma depending on

ther C. berlandieri or

each individual’s pollen load.

Two additional species of beeflies, Heterostylum
robustum and Poecilognathus scolopax (Bombyli-
idae). also visited flowers of Calylophus berlandieri
(Table 5). We observed H. robustum, a hirsute, gold-
en-colored beefly that hovered over the flowers col-
lecting nectar only at midday; most specimens саг-
On the
Poecilognathus scolopax, a cream-colored and less
hairy beefly than Heterostylum,
early morning, landing on the flower and pushing

ried heavy pollen loads. other hand.

foraged mostly in

about halfway into the floral tube, presumably to
reach the nectar. Despite the scarcity of hairs and
their nectar-gathering habits, most individuals of P
scolopax carried some Calylophus pollen, aa
only one carried more than 100 grains (Table :
Both species are effective pollinators, since many
individuals actively forage among plants and con-
tact stamens and stigmas during flower visits.
Poecilanthrax effrenus (Bombyliidae) is a medi-
um-sized, orange and black beefly that divided its
time between the onagrad Calylophus berlandieri
(Table 5) and the composite Thelesperma (Table 8
during the warmest parts of the day. In fact. of all
the beeflies in this analysis collected with pollen
individuals (97%) visited one of

^

loads, 70 of 78
these two plant taxa: only one individual of Poecil-
ognathus scolopax was collected each on Mentzelia
(Table 9) and Argemone (Table 10). In conclusion.
it appears that the beeflies of the Monahans Sand-
hills are either onagrad foraging specialists or com-
posite foraging specialists, or in the case of one
species, generalized enough to visit onagrads, com-

posites, and other taxa.

Beetles ( Coleoptera )

Like beeflies. flower-visiting beetles were most
abundant in the hottest parts of the day. although
we collected some beetles at other times. They are
most significant as floral visitors of Calylophus ber-
landieri (80 individuals of 10 species, 60 of which
carry some pollen; Table 5). where they ate pollen

and other flower parts and regularly contacted the
stigmas. They also fly between plants and are prob-
ably effective pollinators. The beetles Altica sp. in-
det. (Chrysomelidae) and Achmaeodera mixta (Bu-
prestidae) together accounted for 25% (63 of 252)
of all insects collected on flowers of C. berlandieri,
but carried less than 8% of the cumulative pollen
load (Table 5). At least some beetles were collected
on all plant species in our data set, and in all three
non-Onagraceae species (Tables 8-10). at least one
beetle carried a large pollen load. However, beetles
did not cumulatively constitute a major class of
flower visitors or of pollen carriers for апу plant
species other than C. berlandieri. Primack and Sil-
ander (1975) reported beetles as effective pollina-
tors of the day-flowering Oenothera fruticosa L.
(Onagraceae) in North Carolina, although they were
secondary in importance to introduced honeybees
as pollinators. We did not observe beetle larvae

feeding on any plants at our study site.

Moths and butterflies (Lepidoptera)
Butterflies were rare at the Monahans Sandhills
site in western Texas in 1999 and 2000, possibly
due to prolonged drought conditions. Scattered in-
dividuals of five butterfly families visited plants in
our study communities, but in only two instances
were they carrying any pollen. Three individuals of
FEuptoita claudia (Nymphalidae) small
amounts of Thelesperma pollen, and a single male

carried

sachem skipper (Atalopedes campestris huron: Hes-
periidae) carried a major load (> 50 grains) of
Mentzelia pollen, each of them foraging during the
noon to 4 P.M. period.

Moths, on the other hand, were the most common
eroup of insects in our analysis. Four families of
moths (Geometridae, Noctuidae, Pyralidae. and
Sphingidae) are represented in this data sel. and
all limited their flower visitations to species of On-
agraceae, although a few carried pollinia of an un-
known and unseen species of Asclepias (Apocyna-
ceae, Asclepiadoideae) on the tips of their legs.
Even though these four moth families account col-
lectively for 622 of the 1299 total insects collected
(18%). they generally carry small pollen loads: only
59 of these 622 individuals (9%) carry more than
50 pollen grains, our pollen-load threshold for ma-
jor pollinators. This major discrepancy between the
visitor frequency and pollen load in moths may be
a collecting artifact (i.e., pollen is lost from moths
in the capture process more easily than from other
insects), but more likely has a structural explana-
tion.

The pattern of pollen deposition on the bodies of

394

Annals of the
Missouri Botanical Garden

moths found during pollen load analysis differs
from the pattern observed on most other insect vis-
itors. On many insects, especially those that forage
primarily for pollen rather than nectar, we found
most or all pollen on the ventral surface of the body.
Hymenoptera frequently carried massive pollen
loads, concentrated in and around specific pollen-
gathering structures such as corbiculae or scopae.
Most individuals of Coleoptera, Diptera, and Neu-
roptera also carry most or all of their pollen loads
on their ventral surfaces. Some pollen grains also
were found on the head and around the mouthparts
of many insect visitors. However, in all groups of
moths in our sample except the Sphingidae, most
or all of the pollen was found on the proboscis, with
relatively less on the ventral thorax, abdomen, and
legs. This is true even on freshly collected speci-
mens handled carefully to avoid pollen loss. This
relative absence of pollen on the ventral surfaces
of moths may be due to a general lack of hairs and
other epidermal features that might trap pollen on
those body parts, and also to the presence of scales
on Lepidoptera, which may impede pollen adher-
ence. It is unclear whether pollen on the moth pro-
boscises effects pollination as well as that on the
ventral surfaces, but we recorded total pollen pre-
sent (proboscis and ventral body) for all lepidop-
teran visitors.

For the non-sphingid moths in our sample, most
of the pollen load (ca. 85%) adheres to the probos-
cis, with much smaller amounts on the legs (less
than 10%) and ventral thorax and abdomen (less
than 5%). We observed a similar distribution of pol-
len on museum specimens of noctuids and geo-
metrids examined at the Field Museum. Because
most moths land on the staminal filaments while
extending their proboscises to gather nectar, with
the ventral thorax and abdomen pressed against the
anthers and stigma, this lack of ventral pollen is
puzzling. If pollen falls off or even is “dusted” off
during handling of the specimens, one might expect
comparable pollen loss on other types of insects,
and perhaps similar loss of pollen from moth pro-
boscises, but this is not observed. Ventral deposi-
tion of pollen on moths surely must occur, but per-
haps adherence of pollen to moth scales is weak,
at least relative to adherence on insects with hairy
or scabrous ventral surfaces. If so, the pollen loads
counted for moths in our analysis may underesti-
mate the actual pollen carried by the moths, and
underestimate their efficacy as pollinators. А com-
parative experimental analysis of pollen adherence
to insect bodies would be necessary to resolve this
question, and would be very useful for determina-
tion of pollinator effectiveness.

Sphingidae

Commencing at twilight, there is a surge in ac-
tivity of the sphingid moth Hyles lineata on flowers
of Calylophus hartwegii, and to a lesser degree,
Oenothera rhombipetala. Difficult light conditions
and the speed with which these moths move made
catching them a particular challenge. Like other
moths, Sphingidae carry pollen on the proboscis,
but unlike other moths, they also carry substantial
pollen on their ventral surfaces. Nonnenmacher
(1999) observed ventral pollen deposition on sphin-
gid moths visiting Oenothera macrocarpa (Onagra-
ceae) on the Konza Prairie (Riley Co., Kansas,
U.S.A.). This species is rather similar in floral mor-
phology to Calylophus hartwegii, and elicits similar
behavior by the sphingid moth visitors.

Geometridae

Whereas large sphingid moths forage on onagrad

—

axa with long corolla tubes at twilight, small geo-
metrid moths (as well as somewhat larger noctuids
and pyralids) actively visit freshly opened flowers
of Gaura coccinea. Gregory collected moths on this
7:00 P.M
Monahans (sites 4 and 8; Table 1) and the Trans-

species from . until midnight, in both the

sites | and б) in western Texas. In both cas-

—

pecos
es, small moths were most abundant until about 9:
ЗО P.M., after which larger noctuids predominated.
Most of the geometrid moths are an undetermined
species of Semiothisa, which accounts for 47 of 238
insects (20%) caught on G. coccinea flowers. Even
though most carry small pollen loads, they may be
effective pollinators of G. coccinea as they fly
among plants and land on flowers to forage nectar.

Noctuidae

1979)

suggested that noctuid moths are the primary pol-

Raven and Gregory (1972a; also Raven,

linators of most species of Gaura, and our data sup-
port this contention at least in part. The most nu-
merous pollinators of G. coccinea are four species
of noctuid moths and one geometrid; of the nine
major pollinators of G. villosa, two species of noc-
tuid moths, Bulia deducta and Melipotis indomita,
account for 53% of total visitors but less than 10%
of the total pollen load (the other major pollinators
are antlions and bees; Table 11). If, as we discussed
above, the small pollen loads on these noctuid taxa
are an artifact. of collecting and/or curating moth
specimens, then the importance of noctuid moths
as pollinators of these Gaura species may be un-
derestimated in our analysis. However, even if noc-
tuid moths carry only small pollen loads, the sheer

Volume 91, Number 3
2004

Clinebell et al. 395

Pollination Ecology

number of these insects actively moving that pollen
among plants clearly marks them as important and
effective pollinators.

Bulia deducta and Melipotis indomita (Noctui-
dae, subfamily Catocalinae) were active throughout
the night, with an activity peak between 10:00 P. u.
00 a.m. Both of these species exhibited in-
teresting behaviors. At site 9 in Aug. 1999,
viduals of M. indomita came to the vicinity of Oen-
othera rhombipetala plants an hour before sundown
when the flowers open and alighted on the sandy

and 2
indi-

ground, where they were perfectly camouflaged.
This behavior enabled them to visit the flowers as
soon as they burst abruptly into bloom at twilight,
in competition with a dramatic influx of sphingid
It may in fact be essential for Melipotis to

forage at newly opened flowers before the larger

moths.

sphingid moths, with their longer proboscises, take
too much nectar from the long floral tubes of the
Oenothera (20-30 mm; Munz, 1965). Melipotis also
co-foraged with sphingids during the twilight an-
thesis period in Brewster County (site 2 in May
2000) on Calylophus hartwegii, which also has rel-
atively long floral tubes (19.2 mm; Table 3), but we
were unable to observe if they clustered around
plants prior to anthesis. We did not observe either
clustering or co-foraging behavior in M. indomita
when it visited flowers of either species of Gaura
(floral tubes 2.1—5 mm long; Table 3). which are
seldom visited by sphingid moths.

Bulia deducta exhibited two foraging strategies
on Gaura villosa. Commonly, this noctuid moth
alighted upon the staminal filaments and style, and
rested its wings while feeding on nectar. On several
occasions, however, a moth would land on the floral
tube and ovary, below the petals and stamens, and
reach its proboscis between the petals and into the
floral tube without contacting the stamens or stigma
and therefore not effecting pollination. This behav-
ior was observed at site 9 in May 2000, when one
of the largest antlions, Paranthaclisis hagent, was
present. In May 2001, this antlion species was par-
ticularly abundant in the large population of G. vil-
losa at Monahans Sandhills (site 9), and no moths
were present, a most unusual situation for this sys-
tem. Abundant moth scales on the bodies of these
antlions suggest they may be preying on moths at
the same time as they forage for nectar.

Pyralidae

The garden webworm (Achrya rantalis) was the
primary pyralid moth encountered. This species.
collected. on both
(2:30-4:30 A.M.) and before sunrise (5:30-7:00

Gaura villosa after midnight

A.M.), carried hardly any pollen. Like several of the
smaller noctuid moths, these pyralid moths were
shorter than the length of the stamen filaments.
Thus, they could land near the throat of the floral
tube and touch neither the anthers nor the stigmas.
These infrequent visitors may be nectar robbers,
but in any event are not effective pollinators.

Antlions (Neuroptera)

The first antlion of this study was recovered tak-
ing nectar from a population of Gaura villosa just
south of the Kiowa National Grassland ((
Creek patch, Union County, New Mexico, 23 July
1999, 2:00-4:00 X. M.). This female Scotoleon min-

usculus (Neuroptera, Myrmeliontidae) carried about

carrizo

20 pollen grains of Gaura on its legs and ventral
surfaces. Insofar as we know, this specimen appears
to provide the first unambiguous documentation of
pollen transport and pollination by any member of
family Myrmeleontidae. There are several reports
in the literature of floral visitation (nectar and pol-
len foraging without clear pollination) involving
other Neuroptera, especially Sialis (alderfly) and
Hemerobius (brown lacewing) on Apiaceae (Müller.
1883; 1973; 1996).
but in no cases are they reported as anything other
than rare and minor floral visitors. Múller (1883)
reported that only 13 of 5231 (0.2%) pollinator vis-
its he observed involved Neuroptera, and many of

Proctor & Yeo, Proctor et al..

those involved Panorpa, now considered in the or-
der Mecoptera (scorpionflies). This study provides
clear evidence that antlions are major pollinators
of Gaura villosa.

Additional specimens of Scotoleon minusculus
(both males and females) were collected at site 9
in the Monahans Sandhills on Gaura villosa flowers
in Aug.—Sep. 1999, Seven specimens were recov-
7:00 K. M.,

and observed to hover over and land on the flowers.

ered from 5:30 to while it was still dark,
All seven carried Gaura pollen, and four had more
than 100 grains, mostly on the face, legs, and ven-
tral thorax, with a few on the wings (Fig. 3). Six
more antlions were collected from 2:30 to 4:30
v. M., with five carrying more than 100 grains and
two up to 1000 grains. Among this late-night sam-
ple was a male of Vella fallax, the largest antlion
(60 mm long) in North America. This large antlion,
carrying fewer than 10 Gaura pollen. grains but
well-dusted with moth scales, was observed on a
flower in contact with stamens and stigma, sug-
gesting that it may be an effective pollinator, but
also that it may prey on moths. The specimen also
exuded several droplets of clear liquid (nectar?)
from the mouth during the pinning process.

396 Annals of the
Missouri Botanical Garden
кта L Ке.
Figure 3. Female adult antlion, Seotoleon minusculus. showing pollen of Gaura villosa on ventral surface of thorax:

collected at Monahans Sandhills, Ward Co.

During a later trip to Monahans (site 9) in May
2000, we captured more individuals of Scotoleon
minusculus on Gaura villosa, as well as specimens
of three additional species of antlions, and were
able to observe their foraging behavior more care-
fully. Most antlions were captured after midnight,
when their clear wings and slender black bodies
rendered them almost invisible. Typically, S. min-
usculus and Brachynemurus hubbardi spent long
periods hovering around the plants, at a distance
of up to one meter, approaching a flower and then
suddenly withdrawing backward in a straight or el-
liptical pattern, but always facing the Gaura plant.
The antlions landed on the Gaura flower much like
noctuid moths, by grasping the filaments and style
with their legs and crawling up the filaments until
they could bury their faces in the throat of the floral
tube. They sometimes remained in this position for
several minutes. In this process, the ventral surface
of the insect became covered with pollen, which
was absent only from the posterior half of the ab-
domen on the most pollen-laden specimens. We ob-

served as many as six individual antlions around a

Texas (site 9, °

able 1): | Sep. 1999 (photo by R. Keating).

single plant, approaching and retreating before fi-
nally landing on a flower.

possible reason for this apparent reluctance
by the antlions to land became clear when we found
and collected an antlion on a Gaura flower in the
clutches of an unidentified white crab spider (fam.
Thomisidae). We observed crab spiders on several
occasions hiding beneath the petals and ambushing
insects that landed on the flower, which is a typical
and well-documented behavior for this family of
spiders. We collected an additional crab spider and
observed one additional antlion capture by a spider
at site 9 on 20-21 May 2000 in the course of col-
lecting 26 antlions. This suggests that predation of
antlions (and other pollinators) by crab spiders is
not an isolated occurrence in these communities.
and may influence the foraging behavior of the ant-
lions. Our observations also suggest that nectar for-
aging is important enough to antlions to risk pos-
sible predation during flower visitation.

Paranthaclisis hageni, the most abundant of the

three large (> 40 mm in length) antlion species,

also forages for nectar and lands on the Gaura flow-

Volume 91, Number 3
2004

Clinebell et al.
Pollination Ecology

ers just as do the smaller antlions. However, indi-
viduals of P. hageni are so heavy that they bend
the entire inflorescence downward when they land.
This antlion also is less likely to carry байга pollen
and when it does, the pollen load is smaller (Table

2. ANALYSIS OF MIXED POLLEN LOADS

this

Mixed pollen loads are relatively rare ii
analysis, at least compared to other similar recent
1998; Clinebell &
1998: Nonnenmacher, 1999).

fact that all of the taxa studied here commonly oc-

studies. (Clinebell. Bernhardt.

This is despite the

curred together in mixed species stands, with meta-
populations of each plant species usually 50 to
1000 individuals.

loads by shared plant species pairs.

Here we discuss these mixed

Calylophus-Gaura pollen loads

The only insect. visitors carrying these mixed
loads were females of Sphecodogastra danforthi. We
collected this species on both Gaura villosa and
Calylophus berlandieri at the Monahans Sandhills
(site 9) in August 1999, May 2000, and May 2001.
Of the 94 females collected with pollen on C
13 carried Gaura pollen, of which 12 car-
50 Gaura grains out of 200 total
or > 25% (Table 5). Of the 20 fe-

males collected on Gaura, one carried about equal

lophus.
ried more than

grains counted,

amounts of Calylophus and Gaura pollen (Table
The grains of C. berlandieri are smaller, with prom-
inent basal constrictions of the apertural protru—
1988. fig. 16).
larger grains of G. villosa
1988, fig. 2F).

Little pollen of any other plant was recovered on

sions (see Praglowski et al. com-
the

(Praglowski et al.,

pared with

other individuals of Sphecodogastra danforthi, in-
dicating that this bee is a strong oligolege for On-
agraceae (McGinley,
both onagrads was roughly equal, suggesting that
these halictids prefer Calylophus over Gaura; this
Is supported by the fact that we observed the bees
foraging for nectar on the Calylophus, whose flowers
open in the morning. By contrast, Gaura villosa
opens in the evening and its nectar is collected all

night long by moths and antlions.
Calylophus-Thelesperma pollen loads
Two species of beeflies at Monahans (site 9) car-

ried this particular mixed pollen load. Eight of 25
individuals (32%) of Poecilanthrax collected on C.

berlandieri carried such mixed loads. as did two of
y berlandieri

three Exoprosopa sp. Flowers of C.

2003). Morning sampling of

and Thelesperma are borne at about 20-30 dm
height, much lower than those of other co-blooming
laxa except for Gaura coccinea, which does not oc-
cur in the immediate vicinity of most populations
of these two plants. By contrast, flowers of Gaura
villosa, Mentzelia, and Argemone are borne at about
60-120 dm height. This suggests that the beeflies
may prefer to forage among shorter vegetation at
Monahans.

Other mixed pollen loads

The only other mixed load encountered on more
than two individuals of any insect species was a
mixed pollen load of Gaura coccinea and Dalea sp.
indet., found on five of six male anthophorid bees
Martinapis enteicornis) collected on G. coccinea al

sith

site 5 in the Monahans region. Again, these flowers
are held at a height of about 20-30 dm. and may
represent a foraging height preference.

The very low relative abundance of mixed pollen
loads in this large sample of insect visitors was
unexpected and surprising. A possible explanation
may derive from the fact that the data set is so
heavily loaded with onagrad. oligoleges—namelv.
all the anthons, most of the moths and bees (es-
pecially in Sphecodogastra and Evylaeus), and some
beeflies. This paucity of mixed pollen loads is in
spite of careful examination of pollen wash slides
for virtually every individual insect for which a po-
tential for a mixed load existed.

CONCLUSIONS

Our primary study site at the Monahans Sand-

hills

plant community that supports a diversity of insect

western Texas represents а fairly simple

pollen and nectar foragers. Because this is a hot
semi-desert the
heat of the day by foraging from early evening to

community, many insects avoid
early morning, with only a few insect groups active
between 10:00 A.M. and 5:00 P.M. Several plant
species experience intense and predictable periods
of visitation by specific insects, usually coinciding
with the onset of anthesis. An obvious conclusion
and effective

of this study 15 that floral visitation

pollination—can take place throughout the diurnal
cycle, and that some visitors are active only during
the night. Another conclusion is that although each
plant species has one or a few predominant pollen
carrier(s), all species have a diversity of major pol-
len carriers (> 50 grains), including more than one
order of insects in all species except Gaura cocci-
ned.
Tables 11 and 12 indicate that the major pollen

carriers. (all insects carrying more than 50 pollen

398

Annals of the
Missouri Botanical Garden

grains of the plant species in question) in the Mon-
ahans ecosystem are largely non-overlapping
among the seven primary plant species we studied.
In part, this may reflect the floral morphology and
time of flowering in the species of Onagraceae. In
the night-blooming species, those with shorter (1.5—
11 mm) corolla tubes (Gaura spp.) attract mostly
noctuid moths (Raven & Gregory, 1972a) and, in
the surprising case of G. villosa, antlions, whereas
onagrads with longer (16—50 mm) floral tubes (Ca-
lylophus hartwegii) attract more sphingid moths
(Towner, 1977). The day-flowering С. berlandieri at-
tracts day-flying bees and other insects, but not
moths. Even in the day-flowering non-onagrad spe-
cies, there also is little overlap among pollen car-
riers. Few comparable studies that examine floral
visitation rates and pollen load through diurnal and
seasonal cycles are available, so it remains to be
seen if this high degree of pollinator specificity is
the exception or the rule. This report is the first in
a series of analyses of North American plant com-
munities that include Gaura, Calylophus, and other
species of Onagraceae, in which we intend to ex-
amine the evolution of pollination biology in this
group, and to compare the community pollination
biology of these different assemblages of taxa.

Even with our relatively large sample sizes, some
members of the community pollinator guild remain
rare in our data set. This is particularly true for the
largest species in various insect groups, where we
collected only single specimens of two large ant-
lions, an underwing noctuid moth, a beefly, an an-
thophorid bee, and a Euphoria flower beetle, each
the largest taxon in their group. This may simply
indicate that these large pollinators are less com-
mon, but it also suggests that our description of this
guild may be incomplete.

An apparently unavoidable cost in the census of

these rare pollinating species is the collection of
large numbers of the commoner species in the com-
munity. However, understanding the biology and
behavior of these rare taxa and the role(s) they play
in natural communities may be critical to under-
standing those communities. Some of the taxa that
we rare in our analysis may be more common at
other times, for example, when the communities are
not experiencing drought conditions. Pettersson
(1991) found strong year-to-year variation in the
abundance of pollinating moths on Silene vulgaris
in Sweden. We suggest that sustained and detailed
studies that include a moderate amount of repeated
collecting over several years are essential to elu-
cidating the roles of rare species.

n terms of community pollination ecology in
western North America, our results prompt two ob-

fera (see also Primack & Silander, 197

servations: (1) Analysis of pollination guilds is ob-
scured when a study area is overwhelmed by large
populations of the European honeybee, Apis melli-
5). The gen-
eral scarcity of honeybees in our primary study site
in the sandhills of Ward Co., Texas (site 9), dem-
onstrates that the site is relatively pristine, with its
native pollination guild intact. At our site in Brew-
Co. (site 2), however, the invasive honeybee
major pollen carrier of Calylophus

ster
appears as a
hartwegii, a species with apparent specializations
for hawkmoth pollination. (2) Disturbed and de-
graded assemblages of plant species may give a
similarly distorted picture of the pollination guild,
compared with an undisturbed site. Our analysis of
this relatively intact community shows both a high
degree of pollinator specialization and the presence
of a diversity of relatively rare insect visitors as

—

pollinators.

The richness of the data that can be harvested
when studies in pollination ecology span a variety
of co-blooming dominant plants in different plant
families is much more interesting, it appears to us,
than studies that focus on a single species, genus,
1998, 2004). Such
community-level studies give an overview of the

or family (see also Clinebell,

role a given insect species plays in the overall dy-
namic of the community, and the degree of fidelity
enjoyed by a given plant species in the ecosystem.
These comparisons allow the use of statistical anal-
ysis and thus elevate studies of pollination biology
from the status of descriptive natural history into
the realm of hypothesis-driven quantitative ecology,
as well as the identification of probable coevolu-
tionary relationships between plants and insects.

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A SYSTEMATIC OVERVIEW
OF FRANKENIACEAE AND
TAMARICACEAE FROM
NUCLEAR rDNA AND
PLASTID SEQUENCE DATA'

' Farrokh
Dao-yuan Zhang."

John F. Gaskin,
Ghahremani- dc oe
and Jason P. Londo?

ABSTRACT

Within the sister families Frankeniaceae and

Tamaricaceae

(order Caryophyllales) we investigate the systematic

1
plac ement of tape ricopsis, Myrtama, and Hololachna, which have at times been lumped into other genera Frankenia,

amar | Mori and Reaumu
their pre vious taxonomic ee ements and a
regions rbcl. RNAS
support for fon EA ment of Hyperic opsis within Frankenia.
rds: 188. Frankenia. Franken Ho

Tamaricaceae, Tamaricaria. Tamarix. |

aria, ria, respectively) or,

огасппа.

RN

ey 10 ran niaceae,

rbcL, Possit

alternatively,
nalyze sequence data from the nuclear ribosomal region 18

T (GCU)/ URNA С ly (UCC) intergenic spacer for the

retained as small distinct genera. We describe
S and chloroplast
> genera in both lies: finding cladistic
and for Myrtama and Hololac ine as distinct genera.
Hypericopsis, molecular systematics, Myricaria, Myrtama,

А Ser (GCU) tRNA Gly (UCC) intergenic spacer

The plant families Frankeniaceae and Tamari-
caceae consist of halophytic and xerophytic shrubs
and trees, and occasional herbaceous plants. They
have historically been placed as sister families be-
cause they share characters such as secondary
structure, and often petaline
L.. Hololachna
Reaumuria L.). As a group they have, until lately.
1988:

Thorne, 1992) due to their polypetalous flowers and

chemistry. gland

Scales (Frankenia Ehrenb.. and

been in the order Violales (e.g.. Cronquist.
mostly parietal placentation. Recent molecular
analyses (sensu APG, 1998) have moved both fam-
ilies to the Caryophyllales. close to such families
as Droseraceae. Plumbaginaceae, and Polygona-
Lledó et al., 1998; Soltis et al., 2000:
2002), which are caryophyllid fam-
ilies that share a straight embryo and endosperm
(Spichiger & Savolainen, 1997).

families Frankeniaceae and

ceae (e.g..

Cuénoud et al..

The two Tamarica-

ceae have obvious morphological differences in

phyllotaxis (opposite in Frankeniaceae, spiral in
and leaf shape (strongly revolute to

—

Tamaricaceae
almost flattened in Frankeniaceae, flattened or su-
bulate in Tamaricaceae). Molecular studies, such as
those mentioned above, were not focused on intra-
familial relationships, and thus included only one
species from Frankeniaceae and/or Tamaricaceae.
This is the first molecular systematic investigation
within Frankeniaceae, and the first such investi-
gation in Tamaricaceae using multiple independent
loci. Zhang et al. (2000) have previously analyzed
the internal transcribed spacer region (ITS) and in-
tervening 5.85 subunit of the 185-265 nuclear ri-
bosomal DNA for various Tamaricaceae.

The Frankeniaceae currently contain one genus,
Frankenia, which encompasses the monotypic Hy-
pericopsis Boiss. |= Frankenia persica (Boiss.) Jaub.
& Spach]. 1
genera (> 10 species), Tamarix L., Myricaria Desv.,

'amaricaceae presently have three larger

and Reaumuria, and two smaller genera (1 to 2

This work was supported by USDA National Research Initiative Competitive Grants Program, Cooperative State

Education, and Extension Service grant

Research, !
Committee for
Garden graduate students,

To

and an EPA

A. Shehba

members p the > Schaal e ne M. M halen for j" B comments. Specimens were
Ol« J M.

DeLoach, J. Кепе, d

have һе “п oie witho
188

299, St. Lou
? Washington University Ne outs, Campus Вох 1
ei address: USDA ARS NPARL,

sidney.

ars.usda.gov
B enl ‘of Йй

Faculty of Science,

#2000-00836 (B. Schaal and JFG).
` Research and Exploration grant # 0003-99 (JEG). the Me “н Foundation support of Missouri Botanic al
Achieve Results (STA

1500 North Central

University of Tarbiat-Moallem,

National Geographic Society

К) graduate fellowship (JFG). We thank
gr |

kindly donated by A. E nin,

nd Whalen. The collections of Hypericopsis ЖОШ. по!

Шш generous Ве ка of D Fac vlt of OPI vr es at Tehran University in Karaj, Iran.
30x . Missouri 63110, U.S.A.
1137. One Brookings dins ve,

. Louis, Missouri 63130, U.S.A.

Avenue, es d 59270, U.S.A. jgaskin@

19 Dr. Moffateh Avenue, Tehran 15614.

ran.
e South Beijing Road 40-3, Xinjiang Research Institute of Ecology and Geography, Chinese Academy of Science,

830011 Urmgi, Xinjiang, China.

ANN. MISSOURI Bor.

GARD. 91: 401—409. 2004.

402

Annals of the
Missouri Botanical Garden

species), Myrtama Ovez. & Kinzik. and Hololach-
na. Here we discuss the taxonomic history of the
smaller genera, and present nuclear and chloroplast
sequence data analyses in an effort to clarify their
phylogenetic placement.

FRANKENIACEAE

Frankenia contains about 70 to 80 species (Mab-
berly, 1993; Kubitzki, 2003) distributed in many
temperate and subtropical regions on saline or gyp-
seous soils. Frankenia persica, a narrow endemic
from Iran, is found mostly on the salty shoreline
soils of lakes near Shiraz, between 1300 and 1700
m elevation. This species was originally described
as the monotypic genus Hypericopsis containing H.
persica (Boissier, 1845), with 5 to 6 calyx lobes and
6to7
and 5 petals in Frankenia, but note that there are

petals, compared to the usual 5-lobed calyx

more recently described Frankenia species with 5
to 6 calyx lobes (e.g.. К punctata Turez.) or 4 to 6
petals (e.g., А interiosis Ostenf.). Soon after Bois-
sier's original description Jaubert and Spach (1847)
moved H. persica into Frankenia, an action that was
not universally adapted, as the name H. persica is
still often applied (e.g., Chrtek, 1972; Kubitzki,
2003). According to Niedenzu (1925a), F persica
and the rest of Frankenia differ mainly in stamen
number (16 to 24 vs.
petal size (8-12 vs. 5-7 mm), though when consid-
ered worldwide, there are Frankenia with petals up
to 16 mm (e.g.. F cordata J. Blac

3 to 12, respectively) and

TAMARICACEAE

Tamaricaceae contain about 80 species (Mab-
berly, 1993) found in temperate and subtropical Af-
rica and Eurasia on salty or dry areas of deserts,
steppes, sandy shores, and along rivers (Gaskin,
2003). Tamarix is the largest genus in the family,
containing approximately 54 species (Baum, 1978)
that naturally occur in northern Africa and Eurasia.
There are also two disjunct species, 7! angolensis
Nied. (Angola, Namibia, and South Africa) and 7.
usneoides E. Mey. ex Bunge (Namibia and South
Africa). Naturalized species, often severely inva-
sive, are found in the U.S.A, Mexico (mostly T. ra-
mosissima Ledeb. and T. chinensis Lour.) (Ríos &
García, 1998; Gaskin & Schaal, 2002), e ded
tralia (7: aphylla (L.) Karst.) (Griffin et al.,
Myricaria contains about 10 species of cen
(some prostrate) ranging from Europe to mainly
central Asia. The only consistent morphological dif-
ference between these two genera is that there are
10 monadelphous stamens in Myricaria versus 4 to
14 distinct stamens in Tamarix. Myricaria tends to

have sessile, cushion-like stigmas (or at least no
obvious style or style branches) and a stipitate seed
pappus, while Tamarix tends to have a short sty-
lodium and a sessile pappus, but there are excep-
tions (see Baum, 1978: :

M yricaria elegans Royle was originally described
from the Kunawar region of the western Himalayas
(Royle, 1835). This species, now accepted as Myr-
tama elegans (Royle) Ovez. & Kinzik., has 10 sta-
mens, flat leaves, and no obvious style, so its orig-
inal placement in Myricaria was reasonable.
However, the stamens are distinct (vs. monadel-
phous in Myricaria) and the pappus is sessile (vs.
stipitate), which is presumably why Baum trans-
ferred Myricaria elegans to Tamarix in 1966, giving
it the name J. ladachensis Baum (because the name
T. elegans Spach was already occupied). In 1977
Ovezinnikov and Kinzikaeva considered the spe-
cies as intermediate to Myricaria and Tamarix and
placed it in its own genus, Myrtama. The next year,
M yricaria elegans was transferred to another novel
genus, Zamaricaria Qaiser & Ali (1978), nom. il-
legit. Zhang and. Zhang (1984), Tang (1986), Liu
(1995), and Xi (1988) further discussed the taxo-
nomic status of Myricaria elegans citing different
morphological evidence such as pollen and seed
morphology and agreed with its original placement
in Myricaria. Zhang et al. (2000) sequenced the
nuclear ribosomal ITS region for various Tamari-
caceae, and due to high levels of heterozygosity in
Myrtama, proposed that it is either a recent hybrid
of Tamarix and Myricaria, or a long established
intermediate genus. Zhang (2001) investigated pol-
len morphology and supported placement in Myr-
tama.

Reaumuria is a genus of about 12 small shrub
species ranging from Europe to central Asia and is
easily distinguished from all other Tamarix and
Myricaria by its solitary flower vs. clusters and the
presence of lateral scales on the adaxial base of its
petals. In. 1827 Ehrenberg described the new
monotypic genus Hololachna, containing a central
Asian Tamaricaceae with solitary flowers (Hololach-
na songarica Ehrenb.). He placed it there instead
of in Reaumuria because it had a unique 2- to 4-
carpellate ovary, 2 to 4 subulate style branches, and
8 to 10 stamens, instead of the 5-carpellate ovary,
usually 5 filiform style branches, and 5 to many
stamens typical of Reaumuria (Ehrenberg, 1827:

273). Hololachna also has lateral scales on its pet-
als like Reaumuria (Niedenzu, 1925b), though they
are almost indistinct at | mm in length. In 1873
Hooker added Hololachna shawiana Hook. f.
Henders. & Hume (not sequenced herein) to the
genus (Henderson & Hume, 1873). Recent authors

Volume 91, Number 3
2004

Gaskin et al.
Frankeniaceae and Tamaricaceae

(e.g.. Schiman-Czeika, 1964; Mabberly, 1993; FCC,
2002; Gaskin, 2003) have treated Hololachna as

part of Reaumurta.

MATERIALS AND METHODS

We sequenced the tRNA Ser (GCU) tRNA Gly
(UCC) intergenic spacer (IGS) (938 base pairs (bp)
in Frankeniaceae and 765 bp in Tamaricaceae) and
rbcL region (1325 bp) (both from the chloroplast
genome), and the partial 185 region (971 bp) of the
nuclear ribosomal DNA for selected Frankeniaceae
and Tamaricaceae species. Phylogenetic analyses of
the molecular data were used in an effort to clarify
the taxonomic status of the smaller genera.

DNA ISOLATION, AND
SEQUENCING

PCR AMPLIFICATION,

Myrtama elegans, Hololachna songarica, Fran-
kenia (7 species), Tamarix (5). Myricaria (3), and
Reaumuria (4) were sequenced from fresh. silica-
dried tissue. Vouchers (Appendix 1) are deposited
at Index Herbariorum locations, or at the U.S. De-
partment of Agriculture (USDA),
search Service, Grassland, Soil and Water Research
Laboratory, 808 E. Blackland Rd..
76502-9601. U.S.A. (which is not listed in /ndex
All GenBank accessions AY099899

5058 are new sequences obtained for this

Agriculture Re-
Temple, Texas
Herbariorum).

o АҮ09‹
analysis. The sequences for Frankenia pulverulenta

—

„ Limonium arborescens Kuntze, Polygonum sp.
indet.. and Eriogonum flavum Nutt. are from other
studies (the citations GenBank
<http://www.ncbi.nlm.nih.gov/Genbank>). There
were no accessions of Polygonaceae species se-

‘ап be found in

quenced for both 185 and rbcL in GenBank, so we
combined the 185 sequence of Polygonum sp. in-
det. with the rbcL sequence of Eriogonum flavum.
Genomic DNA was isolated using a modified
CTAB method (Hillis et al., 1996). PCR amplifi-
cation of the chloroplast intergenic region between
IRNA-Ser (GCU) and tRNA-Gly (UCC) genes uti-
lized the primer pair trnS (GCU) and trnG (UCC)
of Hamilton (1999) with the following thermocy-
cling conditions: 95°C initial denaturation (2 min.):
30 cycles of 95°C min.). 55°C an-
nealing (min.). 72°C extension (2 min.): and then
32°C termination (5 min.). Amplification of the rbcL
plastid region utilized the primer pair rbeL5FOR

denaturation (

(5'-gtcaccacaacagaaactaaage-3') and rbcL3RE\
(5'-gaaltcaaatttgatctectte-3') (origin of primers un-
known) with the cycling conditions varying only by
an annealing temperature of 50°С.
the partial 188 region of the nuclear ribosomal
DNA the primer 185f (5'-gctaata-

utilized pair

Amplification of

and 188r (5'-ecttacta-

Igtetggacctgg-3') that we designed, also with an an-

cgtgcaacaaaccce-3/)
nealing temperature of 50°С. А 50-pl reaction was
performed for each individual, and PCR products
were purified by agarose gel electrophoresis fol-
lowed by QIAquick Gel Extraction. Kit.
PCR template was sequenced using the dideoxy
chain termination method with ABI PRISM* Dye
Terminator Cycle Sequencing Ready Reaction Kit

Purified

with AmpliTaq DNA polymerase. Specimens were
ABI 373A

quencer following manufacturer's instructions. Se-

electrophoresed in an automated se-
quences generated in this study are available on
GenBank (see Appendix | for accession numbers).
PHYLOGENETIC ANALYSES

Sequences were manually aligned using the soft-
ware Se-Al (Rambaut, 1996). The sequence align-
ments are available upon request from the first au-
thor. Insertion/deletion events were treated as a fifth
base. The tRNA Ser (GCU) tRNA Gly (UCC) IGS
sequences were unalignable between the two fam-
ilies, so that data was used only for the intrafamilial
analyses,

We tested for congruence of data sets with the
partition homogeneity test in PAUP* version 4.063
(Swofford, 2000) (with 500 replicates), and it sup-
ports the null hypothesis that two data sets are con-
gruent (congruence of 185 and rbcL data sets for
interfamilial analysis: P = 0.938 (Fig. 1) as well
as the congruence of 188, rbcL, tRNA Ser (GCU)/
tRNA Gly (UCC) IGS

maricaceae or Frankeniaceae: Р = | (Fig. 2)).

data sets within either Ta-

Parsimony analyses of the data sets were per-
formed using PAUP*. Branch and bound searches
used tree bisection reconnection, collapse, and mul-
trees options, with steepest descent not in effect. Ten
runs of 10.000 replicate fast stepwise-addition boot-
strap analyses were conducted to assess clade sup-
port, with the lowest consensus bootstrap score of
those runs recorded. Templeton tests were performed
by making alternate topologies in MacClade 4.0
(Maddison & Maddison, 2000), using these as con-
then compar-

—

straints in PAUP* heuristic searches,
ing the original and constrained topologies in the
trees tree scores parsimony >nonparametric op-
tion of PAUP*, The range of resultant P values from
the Wilcoxon’s signed rank test (Rolhf & Sokal.
1995) was used to determine the statistical signifi-
cance of the difference in length between the origi-
nal and alternative topological hypotheses (signifi-
cance at P < 0.05 in a one-tailed test). Pairwise

distances (uncorrected “p

distances) for Tamarica-

404 Annals of the
Missouri Botanical Garden

Tamarix usneoides
Tamarix aphylla
Myrtama elegans
Myricaria alopecuroides
Myricaria squamosa
Myricaria bracteata
Hololachna songarica
s] 7! Reaumuria hirtella |
100 — 1 سم‎ Reaumuria turkestanica
grow 12 Reaumuria cistoides -
Frankenia pulverulenta
71 | 64 Frankenia persica
| 1 Frankenia hirsuta
58 Frankenia pauciflora
1 Frankenia serpyllifolia
eee a Frankenia johnstonii
3 Frankenia jamesii
Frankenia salina E
Limonium arborescens

91

Tamaricaceae

Frankeniaceae

Polygonaceae
Figure J. Interfamilial strict consensus cladogram of the a Ea E trees for the 1 IT 188
3 A) and rbcL (cpDN ud “ч set, 417 ste m in length, RI = With the uninformative characters excluded,

— 0.719. Bootstrap percentages are above branches and га АТА ha low. Polygonaceae are represented by a
T of 18S sequence үз 5 sp. indet. and rbcL sequence from Eriogonum flavum.

100 r'Reaumuria turkestanica
26

Tamaricaceae
Reaumuria cistoides

Reaumuria hirtella

4l Lu ‘hna songarica

100 Myricaria alopecuroides

Myricaria squamosa

Myricaria bracteata

Myrtama elegans

Tamarix usneoides

Tamarix aphylla Frankeniaceae

Tamarix aucherana 88 СН

Tamarix parviflora 2 Nq-Frankenia persica

Tamarix ramosissima Frankenia hirsuta
Frankenia pauciflora
rankenia serpyllifolia
Frankenia johnstonii

10 changes
Frankenia salina

Figure 2. 5 0 phylograms for ee о and Frankeniaceae (below), from the combined 185
(nDNA), rbcL (cpDNA), and tRNA Ser (GCU) tRNA Gly (UCC) IGS (cpDNA) data sets. Bootstrap percentages are
above brane dap a decay ЗА s below. The Tamaricaceae aga i is is single most parsimonious tree, 372 steps in
length, RI — . With uninformative characters excluded, = 0.798. The Frankeniaceae i is зе single

94.

most parsimonious tree, 114 steps in length, RI = 0.912. W y. кок мше Ия characters excluded, CI =

Volume 91, Number 3
2004

Gaskin et al. 405

Frankeniaceae and Tamaricaceae

ceae were calculated in PAUP*, and are listed in
Appendix 2.
RESULTS

FRANKENIACEAE AND TAMARICACEAE

The two combined 185 nrDNA and re cpDNA
data sets consist of 2296 aligned bases, of which
297 (12.9%) are variable and 172 (7.5%) are phy-
with 80 (0.2%) of the

data matrix cells scored as missing. Excluding the

logenetically informative,
outgroups Plumbaginaceae and Polygonaceae, 187
(8.1%) sites are variable and 65 (2.8%) are poten-
tially phylogenetically informative. The combined
data set vields four most parsimonious trees (not
shown) 417 steps in length (RI = 0.895). When тч
uninformative characters are excluded, CI = 0.7
The interfamilial consensus tree is presented p
Figure 1. In a more rigorous test we searched for
the shortest tree that could violate the constraint of
a a monophyle tic Frankeniaceae. The best topology

steps longer, and the null hypothesis of these
two topologies being statistically similar is rejected
(P < 0.0001 in a Templeton test).

Using only 185 and rbcL data, phylogenetic res-
olution is low within Frankeniaceae and Tamari-
caceae. To improve this, we added data from the
¡RNA Ser (GCU) tRNA Gly (UCC) IGS. As this
IGS region proved to be unalignable between fam-
ilies, we performed two separate intrafamilial anal-
yses based on the 185, rbcL, and tRNA Ser (GCU)
tRNA Gly (UCC) IGS, one for each family.

trees are presented in Figure 2, and they are rooted

These
to preserve the topology in Figure 1.

FRANKENIACEAE

The three combined 18S, rbcL, and the tRNA
Ser (GCU) tRNA Gly (UCC) IGS data sets consist
of 3234 aligned bases, of which 104 (3.2%) are
variable and 40 (1.2%) are phylogenetically infor-
mative, with 15 (0.0%) of the data matrix cells
scored as missing. The data sets yield a single most
parsimonious tree 114 steps in length (RI = 0.912):
Cl =

0.894. This intrafamilial tree shows strong support

with uninformative characters excluded,

(bootstrap support (bs) = 100%) for Frankenia per-
sica within the genus Frankenia (Fig. 2).
TAMARICACEAE

rbcL, and tRNA Ser

The three combined 185,

(GCUY tRNA Gly (UCC) IGS data sets consisted of

3061 aligned bases, of which 277 (9.0%) are var-
iable and 217 (7.1%) are phylogenetically infor-
mative, with 122 (0.3%) of the data matrix cells

scored as missing. The combined data sets yield a
single most parsimonious tree 372 steps in length
(RI =

cluded, CI

0.921); with uninformative characters. ex-
0.798.

sented in Figure 2, shows strong support for 7a-

This intrafamilial tree, pre-

marix and Myricaria as distinct, monophyletic
genera (bs = 100%, P < 0.0001 in Templeton tests
for both genera). Reaumuria is supported as mono-
phyletic (bs = 100%, P = 0.0007 ‘Templeton test)
2) with Hololach-

na songarica appearing as sister to this clade.

in the intrafamilial analysis (Fig.

DISCUSSION

FRANKENIACEAE AND TAMARICACEAE

The interfamilial consensus tree is presented in
Figure 1. As was expected, Frankeniaceae and Ta-
maricaceae are each well supported separate
clades (100% and 91% bs, respectively, and P <
0.0001 in a Templeton test). The molecular analysis
corroborates the earlier morphological data (such as
secondary chemistry, gland structure, and often pet-
aline scales) used as evidence of the close rela-
tionship of the two families. The four most parsi-
monious trees (not shown) for which we show the

—

consensus in Figure 1 vary in the placement o
Frankenia pulverulenta (which remains closest to or
within the Asian and Australian. Frankeniaceae
species) and А salina 1. M. Johnst. (which remains
closest to or within the American Frankeniaceae
species), but neither case affects the following dis-

cussion,

Hypericopsis [= Frankenia persica|

Frankenia persica falls within the other Franken-
ia in the interfamilial analysis (Fig. 1). In the in-
trafamilial analysis, there is strong support for К
persica being in the Eurasian and Australian Fran-
kenia clade (bootstrap = 100%), with the New
World species forming a more distantly related
group (Fig. 2). This clustering of Asian/Australian

American Frankenia, even though for a small
set of taxa. is a useful corroboration of the molec-
ular data sets. When we create an alternative to-
pology in which А persica is outside of the Fran-
kenia clade in the interfamilial analysis, it is
(barely) not statistically different in the rigorous
Templeton test (P = 0.0588), but given the strong
bootstrap support for inclusion of K persica in the
Eurasian and Australian Frankenia in the intrafa-
milial analysis (Fig. 2), we confirm V persica, nol
Hypericopsis persica, as the proper cladistic desig-
nation for this species. The more numerous stamens

(16 to 24 vs. 3 to 12) and larger petals (8 to 12 vs.

406

Annals of the
Missouri Botanical Garden

normally 5 to 7 mm) of V. persica appear to have
been derived from an ancestral Eurasian Frankenia

species,

Tamarix and affined genera

The intrafamilial data set shows strong support
for Tamarix and Myricaria as distinct, monophylet-
ic genera (Fig. 2). The three Myricaria species (Ap-
pendix 1) that we sampled are, as a clade, well
supported as distinct from Myrtama (bs = 100%),
and Myrtama is closer to Myricaria than Tamarix
(pairwise distance from Myrtama to Tamarix is
0.023 to 0.026, while pairwise distance from Myr-
tama to Myricaria is 0.012 to 0.013; see Appendix

. Myricaria species sequenced here are much
c (е to each other than they are to Myrtama (the
greatest pairwise distance within the three Myri-
caria exemplars (0.002) is six times smaller than
the pairwise distance between Myrtama elegans
and the closest Myricaria (M. bracteata) (0.012):
(2000) originally
the ITS
nrDNA sequence of Myrtama elegans using DNA

see Appendix 2). Zhang et al.

found a high level of heterozygosity ir

—

extracted from dried herbarium material. Here, we
used fresh leaf material for DNA extraction and
found no evidence of heterozygosity in our Myrtama
nuclear sequence data, supporting the second hy-
(2000) that Myrtama is an
intermediate genus between Tamarix and Myricar-

pothesis by Zhang et al.

ia, and not a recent hybrid of the two genera. Given
the current molecular data and the morphological
intermediacy of Myrtama (10 stamens and sessile
stigmas, as in Myricaria, but also the stamens are
distinct and the seed pappus is sessile, as in Ta-
marix), we find support for Myrtama as a distinct
genus. Others may wish to include Myrtama within
a Myricaria sensu lato or a Tamarix sensu lato, but
they should note that both molecular and morpho-

logical data would place Myrtama as the outlier of

either group.

Reaumuria and Hololachna

Reaumuria is strongly supported (bs = 100%) as
monophyletic in the intrafamilial analysis (Fig. 2)
with Hololachna songarica appearing as sister to
the rest of the genus. The greatest pairwise se-
quence variation (Appendix 2) between R. cistoides,
К. hirtella, and К. turkestanica (0.017) is very sim-
ilar to the smallest pairwise distance between H.
songarica and any of our three Reaumuria (0.021).
Given the morphological peculiarities of H. son-
garica compared to Reaumuria (2- to 4- vs. 5-car-
pellate ovary, 2 to 4 subulate vs. 5 filiform style
branches, and 8 to 10 vs. 5 to many stamens) and

our molecular placement of H. songarica outside of
the clade containing three species of Reaumuria,
we agree with Ehrenberg (1827) and Niedenzu
(1925b) and consider Hololachna as a separate ge-
nus. Others may wish to include Hololachna within
a Reaumuria sensu lato, but it should be noted that
current molecular and morphological data would
place Hololachna as the outlier of that group.

CONCLUSIONS

In our molecular analysis Frankeniaceae and Ta-
maricaceae are each monophyletic and retain their
sister-family status as monophyletic taxa. This cor-
roboration with earlier morphological data strength-
ens our phylogenetic understanding of the two fam-
Myrtama
elegans, and Hololachna songarica have each been

ilies. In the past, Frankenia | persica,
placed within their larger sister genera or alterna-
tively each has been considered a separate genus,
with morphological support for both cases. In Fran-
keniaceae we find strong molecular support for the
inclusion of А persica within Frankenia, confirming
Frankeniaceae as a monotypic family. In Tamari-
caceae we find strong molecular support for Myr-
tama being separate from Myricaria and Tamarix,
as well as for Hololachna being separate from
Reaumuria, though in both cases these taxa could
also be considered outliers within each sister genus
sensu lato.

Ongoing and future morphological and molecular
research should lead us to a point of taxonomic
stability within the two families. Of special interest
are other Frankeniaceae genera such as Antho-
bryum Phil., Beatsonia Roxb., and Niederleinia Hi-
eron., which, based on morphological data, are now
considered to be within Frankenia (e.g., Whalen,
1987).

analysis, but we hope to test their current place-

These taxa were not available for molecular

ment in future studies. Also, a molecular systematic
analysis of Frankenia from Australia (where 46 of
the approximately 70 to 80 species are found) is
being undertaken by A. Craigie (Whalen lab, Flin-
Adelaide, Australia).

Recent work in Tamarix includes molecular ev-

ders Univ.,

idence of hybridization of phylogenetically diverse
invasive species in the U.S.A. (Gaskin & Shafroth,
in prep.) and a discussion of Tamarix biogeography
(Zhang et al., 2003). Also, a more complete molec-
ular phylogeny of Tamarix (Gaskin, unpublished
data) is under way, including taxa from western Af-
rica and southern Asia.

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Annals of the

408

Missouri Botanical Garden

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Volume 91, Number 3

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Frankeniaceae and Tamaricaceae

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REVISION OF THE
MADAGASCAN ENDEMIC
STAPELIANTHUS
(APOCYNACEAE) BASED ON
MOLECULAR AND
MORPHOLOGICAL
CHARACTERS!

P. V. Bruyns? and С. Klak?

ABSTRACT

The genus Stapelianthus Choux (Ase le pladoideae-Ceropegieae), which is endemic to the arid southern parts o
is

Madagascar, is revised and seven species
chloroplast gene region (¢rnL-trr

1 its present ‹

E

inet e
‘ters separati

species of 5 form a dis
there are relatively charac

synonymy under 5. arenarius Bosser & Morat and 5.
Bertrand. Lec adn s are selected for S. insignis 1 8
Key words:

2F) and one nuclear gene region (ITS
‘ircumscription, Stapelianthus is a monophyletic entity. The molecular characters clearly suggest that the
mary lineage from the remainder of the stapeliads in Africa.
g the species. Consequently, within the genus the relationship:
largely unresolved. Mt are weakly 5 where they are resolved.
diffio ult to circumscribe, it is defined by its unique coronal structure. Stape pa calcarophilus Morat i
dyi Lavranos under S.
nd S. decaryi Choux
Apocynaceae, Madagascar, phylogeny, баре шума.

are recognized, Morphologic ‘al characters and characters derived from one

) are used in a combined analysis to show that,

However,

—
-
7
-
Ф
=
2

Although the genus remains morphologically
s placed in
S. montagnacii (Boiteau) Boite au & Jean

The stapeliads of Madagascar have been some-
what neglected. This is despite the fact that pub-
lications on Madagascan plants have been appear-
ing since the middle of the 17th century, and
therefore one must assume that botanical explora-
tion of the island began even before this. Succu-
lents have not been ignored, and it seems that the
rich variety of aloes has been investigated and writ-
te n about at least since early in the 19th century.

The first species of stapeliad was discovered by
Raymond Decary, provincial Commissioner of the
southern district of Madagascar, in January 1918
near Beloha (P records). This was the very unusual
plant described as Trichocaulon decaryi Choux in
1932. Within ten years of his first discovery of a
stapeliad, Decary had found another two, one near
Ambovombe and another near Fort Dauphin. The
first of these was described as Stapeliopsis mada-
gascariensis Choux in 1931 but, pe the generic
name had already been used by N. S. Pillans in
1928, Stapeliopsis Choux was шл. Choux
then moved this species to a new genus, Stapelian-
thus Choux (in White & Sloane, 1933), and in 1934
he described the third species found by Decary as
Stapelianthus decaryi Choux.

After

this, it was some years until Pierre Mon-

tagnac, Chief of the provincial agricultural service
1 Tulear, discovered S. montagnacii (Boiteau) Boi-
teau & Jean Bertrand in 1940 near Tulear and, in
1957, showed flowering specimens of the remark-
able S. insignis Descoings to Bernard Descoings,
who was then the resident botanist in Tananarive.
It is in this area, i.e., the southwest and west, where
further species have been found more recently.
Stapelianthus has never been accurately defined,
and this may have led P. Boiteau to describe S.
montagnacii first as a member of Stapelia L., an
error which was fairly soon rectified. Subsequent
confusion also arose when R. A. Dyer (1966) moved
Stapelia choanantha Lavranos & H. Hall to Sta-
pelianthus, and Leach (1968) followed along soon
afterward with Stapelianthus baylissii L. C. Leach,
a species which is closely allied to S. choanantha.
Both of these are native to the Cape Province of
South Africa. Rauh and Wertel (1968) showed quite
clearly that these two species had little in common
with the Madagascan species of Stapelianthus, but
only in 1978 were they moved to Tridentea by
Leach (Leach, 1978) and Stapelianthus was once
more restricted to species endemic to Madagascar.
Decary's earliest discovery, the peculiar Trichocau-

lon decaryi was transferred to Stapelianthus in

! This work was in part supported by a grant from the University of Cape Town Research Fu

? Bolus Herbarium, University of Cape Town, 7701 Rondebosch, South Africa. 5 uct. ac. za.

ANN. MISSOURI Bor. GARD. 91:

410—437. 2004.

Volume 91, Number 3
2004

Bruyns & Klak
Revision of Stapelianthus

1961 so that this then became the only genus of
stapeliad represented on the island.

When describing Stapeliopsis madagascariensis,
Choux (1931) mentioned that the organization of
the flower approaches that of Caralluma R. Br.
Br.) and
that the general impression is similar to that of Sta-

(with the corona as in C. dependens N. К.

pelia. His account (Choux, 1934) of Stapelianthus
decaryt was extremely detailed, but there he did
not discuss further the relationship with other Af-
rican stapeliads or make clear what characteristics
are shared by the two species he placed in Stape-
lianthus. White and Sloane (1937) suggested that
Stapelianthus is most closely allied to Huernia and
they stated how, in their opinion, the two genera
differed.

Huernia,

As evidence for the relationship with

they mentioned the “leafless” stems, their
“appearance” and habit of growing in “large crowd-
ed tufts”

very base of the stems”

|S. decaryi|, the “small fascicles at the
in which the flowers arise
and in the flowers the “tubular to campanulate
shapes, with the inner corolla surface papillate”
“sinuses between the corolla lobes pro-

(White &

Sloane, 1937: 961). This view appears to have been

and the
jected into small intermediate points?

reinforced subsequently by the discovery of species
such as 5. insignis and S. keraudreniae Bosser &
Morat, which have considerably extended the range
of corolla shapes found in Stapelianthus and re-
vealed unexpected further parallels with Huernia
R. Br. (compare flowers of H. erectiloba L. C. Leach
and 5. Н. zebrina М. К.
dreniae). The inclusion of 5. pilosus Lavranos & D.

insignis; Br. and S. oi:
S. Hardy in Stapelianthus seemed to substantiate
this relationship yet further since, as White and
Sloane (1937)
stems of this species are very suggestive of those
of Huernia pillansii N. E. Br. Thus Leach (1988: 3)

considered that Huernia and Stapelianthus were

already indicated, the remarkable

most closely related among the stapeliads, though
he also expressed the novel view (presented without
evidence) that Tavaresia was related to both.

The genus Stapelianthus was reviewed by Morat
(1994, 1995) and Rauh (1998). Both authors rec-
ognized nine species and one subspecies. However,
neither of these authors assessed critically the re-
lationships of Stapelianthus to the other genera of
the stapeliads, and they both reiterated the view of
White and Sloane (1937) that Huernia is the closest
relative of Stapelianthus, without presenting any
new evidence for this.

Meve and Liede (2002) included a single species
of Stapelianthus (5. decaryi) in their molecular sur-

vey of the stapeliads. However, their results (e.g..

their fig. 4) did not resolve its relationships to other
genera.

Many of the features mentioned by White and
Sloane (1937) and other authors are common to a
broader range of genera than just Huernia and Sta-
pelianthus, and this is also true of other characters
This leads one te

that were not considered before.
suspect that Huernia is possibly not the closest liv-
ing relative of Stapelianthus. However, our survey
of morphological features did not throw enough

ight on the relationships of Stapelianthus or on the
relationships within the genus. Consequently, we
undertook a molecular investigation, using all the
species in the genus, with characters of one chlo-
roplast gene and one nuclear gene.

therefore.

This study aims, by using both mor-

phological and molecular characters, to address

three issues: is Stapelianthus monophyletic, to
which genera is Stapelianthus most closely related,
and what are the relationships among the species

of Stapelianthus.

MATERIALS AND METHODS

Material was examined from the herbaria BM,
BOL, К, MO, P. PRE, and TAN. For the SEM fig-
ures, material from living specimens was prepared
as described in Bruyns (1993).

INGROUP AND OUTGROUP SAMPLING

For the molecular analysis the seven species of
Stapelianthus that are recognized here were includ-
ed. Traditionally it has been assumed that Huernia
is most closely related to Stapelianthus (White &
Sloane, 1937). Exemplars were therefore chosen in
the tribe Ceropegieae of the Asclepiadoideae from
Huernia as well as from Ballyanthus Bruyns, Du-
valia Haw., Duvaliandra M. G. Gilbert, Orbea
Haw., Tavaresia Welw., and Tridentea Haw., since
these were all shown in Bruyns (2000) to be pos-
sibly related to Stapelianthus. In addition, these are
chosen as a broad sampling from the large, unre-
solved clade to which Stapelianthus belongs in
Liede and Meve (2002, fig. 4). Although Huernia
is the largest genus among the stapeliads (Leach,
1988), only a single species was used here since
recent work (Nowell et al., unpublished) shows that
Huernia is monophyletic. These recent investiga-
tions (Nowell et al., unpublished) included three
species of Tridentea (in the strict sense of Bruyns,
1995), namely, J. marientalensis (Nel) L. C.
T. peculiaris (C. А. 8 L.
Br.) L. C.

this genus is also dedu

Leach.
Leach. and
virescens (N. E. Leach, and found that
This did not cor-

roborate the results of Meve and Liede (2002. fig.

Annals of the
Missouri Botanical Garden

4), where 7! virescens is nested within Orbea, and
it is strongly suspected that this is a consequence
of misidentified material (since no voucher exists
for their Т! virescens). Therefore, here again a single
species of Tridentea is included. These same stud-
ies, as well as that of Meve and Liede (2002), show
that Duvalia is not monophyletic and that the
monotypic Ballyanthus is nested within it. Conse-
quently, two species of Duvalia (D. maculata N. E.
Br. from southern Africa and D. sulcata N. E. Br.
from Arabia) have been included here. In addition,
representatives of more distantly related genera
(Baynesia Bruyns, Caralluma, Echidnopsis Hook.
f., and Rhytidocaulon Р. R. О. Bally) were included.
Riocreuxia flanaganii Schltr., a leafy, non-succulent
member of the Ceropegieae that is sister to many
of the more highly succulent members (according
to Meve & Liede, 2002) was used to root the tree.
Altogether, 21 species were included in the anal-
ysis (see Table 1).

DNA EXTRACTION AND AMPLIFICATION OF
TEMPLATE DNA

Total DNA was isolated from fresh stem material
of the 21 species by the method of Saghai-Maroof
et al. (1984) as modified by Doyle and Doyle
(1987).

The two DNA regions were amplified from total
DNA by the polymerase chain reaction (PCR). The
trnL-trnk and ITS] regions were amplified using
1991) and primers
KI8RC

Hedderson, un-

primers c and f (Taberlet et al.,
182 (Baldwin, 1992) and
GCACGCGCGCTACACTGA-3',

Twenty-five-wl reactions

(5'-
published), respectively.
were prepared, which contained 19.625 wl of ster-
ile water, 2.5 wl of 10X PCR buffer, 1 ul of 10
mM dNTPs in equimolar ratio, 0.75 pl of 10 uM
mM MgCl, 0.125 wl of Taq
DNA polymerase (5 U/pl), and 0.5 wl of genomic
DNA. In general, a LOX dilution of the extraction

primer, 0.5 pl of 25

product was used as template DNA. The thermal

reactions were carried out as follows: first 2 min.
at 97°C to ensure denaturation of double-stranded
template DNA, 1 cycle; denaturing step of 97°C for
for 60 sec., and

min., annealing step of 52°C
extension step of 72°C for 2 min.; the preceding
three steps were repeated 30 times and were finally
followed by one extension step for 7 min. at 72°C
to complete unfinished DNA strands. The reactions
were cleaned using the Ql Aquick PCR purification
kit from Qiagen, and the purified products were
eluted in 30 pl of TE.

SEQUENCING AND ALIGNMENTS

Both strands of the PCR products were cycle se-
quenced, as per manufacturer's instructions, using
the ABI PRISM Dye Terminator Cycle Sequencing
Ready Reaction Kit from PE Biosystems. The prim-
ers used for the amplification were also used for the
sequencing reactions. In addition, for some samples
the internal trnL-trnF region primers d and e were
used (Taberlet et al., 19
on an Applied Biosystems 377 automated DNA se-

The samples were run

files were assembled and edited using
Chromas Version 1.43 (McCarthy, 1996-1997) and
GeneDoc (Nicholas & Nicholas, 1997). Sequences
were aligned by eye. Ambiguous positions were
coded using appropriate IUPAC ambiguity symbols
so as to maximize the retention of information. Gaps
were coded as suggested by Simmons and Ocho-
terena (2000). Their method of simple indel coding
is followed in this study. The alignments of the se-
quences are available from the authors in. Nexus
format.

CLADISTIC ANALYSES

The data matrix was analyzed using PAUP* ver-
sion 4.0b4a (PPE) (Swofford, 2000) under the max-
imum parsimony optimality criterion. with all par-
simony-uninformative characters excluded and all
characters unordered. Initially, each DNA region
was analyzed separately. The first step in each of
these analyses involves an initial sweep of the tree
space in an attempt to increase the chances of iden-
tifying all islands of most parsimonious trees. For
this, one thousand consecutive heuristic searches
were conducted using random stepwise taxon ad-
with (TBR)
branch swapping, MULTREES and steepest de-

dition tree-bisection-reconnection

scent in effect. Branches of zero length were col-

apsed. During each replicate only two trees were
saved. All of these trees were then used as starting
trees for the next search with TBR branch swap-
ping, MULTREES and steepest descent in effect.
Again, branches with maximum length of zero were
collapsed. To assess clade support, the data set was
analyzed using the jackknife option as implement-
ed in PAUP*, Farris et al. (1996) have shown ра
with a removal probability of 36.79%
Backlund & Bremer, 1997) jackknife values of
more than 63% correspond to a node supported by
t least one uncontradicted character. Therefore,
" percentage of deleted characters for all jack-
knife analyses in this study was fixed at 36.79%.
Only groups with frequency greater than 50% were
retained. Nodes with jackknife values greater than

413

Bruyns & Klak

Volume 91, Number 3

2004

Revision of Stapelianthus

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414

Annals of the
Missouri Botanical Garden

or equal to 63% are regarded as supported by the
data (Farris et al., 1996; Backlund & Bremer,
1997; Bakker et al., 1998)

The separate analyses showed that there were no
areas of conflict between the data sets. Where dif-
ferences existed, these were statistically poorly
supported. Therefore, in addition to the separate
analyses, the following combined analyses were
performed. These used the same PAUP settings as
the individual analys

COMBINED ANAL YSIS l.
of the trnL-trnF and ITS] was constructed for the
2] taxa.

COMBINED ANALYSIS 2. A data set consisting

of the trnL-trnF, ITS1, and 19 morphological char-

A data set consisting

acters (as given in Table 3) was constructed for the

21 taxa.

MORPHOLOGICAL CHARACTERS AND THEIR CODING
(NUMBERED AS IN TABLE 3)

Stems

Macroscopic observations

1. Stems erect to shortly decumbent = 0; prostrate

Stems in Stapelianthus are procumbent in most
species, often with ascending apices, though plants
tend to become more decumbent if more exposed
to sunlight (those deeply hidden in bushes main-
taining the most horizontal habit). Only in S. de-
caryt are they decumbent-erect with a shortly pros-
trate base.

The stems tend to form dense clumps, in S. mon-
tagnacii and S. decaryi up to | m or more in di-
ameter, in others rather smaller (up to 0.3 m), and
only in 5. pilosus do they usually form rather diffuse
clusters. Rhizomatous stems (i.e.,
derground stems) do not occur.

horizontal, un-

2. Stems 4- or 5-angled = 0; 6- or more-angled

The tubercles are arranged along the stems in 4
or sometimes 5 angles in Stapelianthus arenarius
Bosser & Morat. S. montagnacii, S. insignis, and S.
keraudreniae. In S. arenarius the angles are not
very clear, but in the others the tubercles are joined
into wings along the stems, which are thus notice-
ably square. In S. madagascariensis the tubercles
are arranged into 4 to 6 angles, which in southern
localities (e.g... Ambovombe to Tsihombe) often
have a slender, rather cylindrical appearance, and
in 5. decaryi into 6 up to 8 angles. In both of these
the primary tubercles are paired and for the first

few nodes the stem is 4-angled, while only later are
the tubercles arranged in alternating whorls of 3 (or
4).

In S. pilosus the rather small, conical tubercles
are densely packed on the stems with no discern-
able arrangement into angles. Seedlings of this spe-
cies have not been studied to find out how this
arrangement begins. In this species the stems are
uniformly green (uniformly purplish if exposed to
sunlight) and smooth.

In the others the stems are mottled with purple-
brown on a cream to silver-gray or greenish back-
ground. In all of these except S. decaryi the surface
is bullate (most markedly so in S. arenarius), es-
pecially toward the edges of the tubercles. In all of
them, including S. decaryi, the tubercles are broad
and somewhat flattened, narrowing abruptly into the
leaf. In most cases the tubercle has a groove on the
upper surface toward the base.

Although variable in thickness (from 3 to 15
mm), the stems are generally slender in comparison
with most African stapeliads (except for those of S.
pilosus, which more closely correspond to other Af-
rican species in thickness).

Microscopic observations of the epidermis of the
stem (Fig. 1)
3. Surface of stem not bullate = 0; bullate = 1.

The bullate surface of the stems of many Stape-
lianthus is most unusual. On the African continent
this phenomenon is rare among stapeliads, where
it is known only in Echidnopsis leachii Lavranos,
the recently Baynesia lophophora
Bruyns, and the few species of Rhytidocaulon P. R.
О. Bally. Bullate stem surfaces are, however, found

described

in many asclepiads from Madagascar: many of the
succulent and practically leafless species of Cy-
nanchum from Madagascar exhibit it, as do also
several highly succulent species of Ceropegia, both
from the arid southwest and elsewhere on the is-
land.

In Stapelianthus pilosus the epidermal cells on
the tubercle are irregularly shaped with flat outer
walls. On the leaf, the cells are long and narrow,
each with a conspicuous, rounded papilla toward or
at the upper end (toward the tip of the leaf).

In the other species examined (S. insignis, S. ker-
audreniae, S.

madagascariensis), the epidermal

cells are + isodiametric, often raised into a low,
rounded, central papilla with a few cells raised into
conical papillae along the edge of the leaf toward
its base. Other cells on the leaf are + as on the
tubercle.

Volume 91, Number 3 Bruyns & Klak 415
2004 Revision of Stapelianthus

Figure 1. SEM views of surfaces of stems and leaves of t e S. pilosus (PVB 5959):—A. Surface of
“leaf "—B. Surface of tubercle with stoma. С. S. arenarius (P 24), leaves and wrinkled surface of tubercle. =
D. S. insignis (PVB 5957), leaves and wrinkled surface of tuberc le. a S. madagascariensis (PVB 5958), stomata aod
cells with flat outer walls. —F. S. keraudreniae (mate m ex hort.). stomata and cells with outer walls with small central
papillae. Scale bars: А. 50 um: В. 100 um: C. 0.6 mm: D, | mm: E, F, 25 um.

Leaf rudiments until eventually falling off. Initially erect, the leaf

l ) 8 1

rudiment gradually spreads with the growth of the

—

Leaf or leaf rudiment clearly differentiated from . мии
та i tubercle. In all species except 5. pilosus. the stron-

the apex of the tubercle (if present) = 0: not

енй dad frin Me apex of the ш ger growth of the upper surface of the tubercle
€ [s € 4 "

pushes the leaf rudiment into a descending posi-
tion.

Leaf rudiments are present in all species, but are In Stapelianthus pilosus the tubercle tapers grad-
always very small and are not clearly differentiated ually into a slender, filiform, + cylindrical leaf ru-
from the apex of the tubercle. They dry out rapidly diment 2.5-4.0 mm long whose base is clearly

persist as a whitish husk (for a long time in marked by the beginning of the small papillae men-

bercle =

Stapelianthus pilosus, in the others more fleetingly) tioned above. In S. decaryi the leaf rudiment is nar-

Annals of the
Missouri Botanical Garden

side with dark purple-red/brown on a creamy or
yellow background. In Stapelianthus montagnacti
most of the flower is uniformly colored inside and
only in the base of the tube is it mottled, while the

rowly conical, slightly flattened above, and 2—4 mm
long. In all the others it is a small, ovate-lanceolate
to narrowly deltoid (narrowly lanceolate in S. ar-
enarius) structure 1-2 mm long, which is flat on the

upper surface and keeled below and merges with
the apex of the tubercle (perched on the broad apex
of the tubercle in S. arenarius). There is no trace

of blade or midrib in any of them.

5. Stipular denticles or stipular gland present — 0:

absent —

Stipules are absent throughout Stapelianthus.

Inflorescences
6. Inflorescences borne toward the apex of the stem
= 0; toward the base = 1.
Inflorescences numerous per stem = О; one per

stem =

In Stapelianthus inflorescences arise near the
base of the younger stems and so are usually found
toward the outer edge of the clump or + on top of
the mat. Several flowers are borne in very slow suc-
cession, usually with only one flower in a given
inflorescence opening at a time. There is rarely
more than one inflorescence per stem. The orga-
nization of flowers in the inflorescence is typical of
simple stapeliad inflorescences, as for Echidnopsis
(Bruyns, 1988). The inflorescences may be some-
what sunken into the stems in 5. arenarius, but they
are otherwise superficial. The bracts are lanceolate
to deltate and rarely possess very small lateral out-

growths toward the base.

Flowers

Corolla

8. Corolla + rotate with small tube = 0; campan-
ulate to tubular —

9. Corolla without distinct thickening around
mouth of tube = 0; with at least somewhat

thickened annulus around mouth of tube = I.

There is a remarkable degree of variation in the

geometry of the corolla within this small genus of

seven species. From nearly flat in Stapelianthus ar-
enarius, shallowly campanulate (S. madagascarien-

sis) to more deeply campanulate (S. montagnacit),
it is modified to rotate with a conspicuous annulus

in S. keraudreniae, bicampanulate in S. insignis,
and deeply tubular in 5. decaryi.

The flowers vary between 10 and 35 mm in di-
ameter and so are neither large nor very small. Most
of them are variously spotted both inside and out-

exterior is often mottled as well.

The outer surface
is smooth, but the inner surface is papillate in all
species. In S. decaryi the inner surface is densely
covered with stout, columnar papillae each with a
black summit, whose apical cell is modified into an
acute seta. In S. montagnacii, S. madagascariensis,
and, to a lesser extent S. pilosus, the papillae are
long and slender. They form quite a dense beard
on the lobes at least in S. montagnacii and are more
scattered in the other two. The apical seta on each
papilla is obtuse in 5. madagascariensis and spher-
ical in S. montagnacii. In S. keraudreniae small,
scattered. papillae are found all over the corolla
with longer ones only toward the edges of the lobes;
in S. insignis small, conical papillae are located
around the edges of the lobes only.

Several species exhibit a thickening of the co-
rolla around the mouth of the tube. Only in 5. in-
signis and most noticeably in 5. keraudreniae does
this lead to a definite annulus, which is the most
conspicuous feature of the flower in the latter.

Gynostegium

О. Outer and inner corona partly fused on sta-
minal tube = 0; UM on staminal tube

and not at all fused —
1. Outer corona lobes not exceeding height of gy-
= 0; much exceeding height of gy-

—

nostegium =
nostegium =

12. Outer corona [би not laterally fused to one
another = О; laterally at least somewhat fused

to one another = 1.

Stapelianthus pilosus is the only species of Sta-

which the outer corona lobes are

—

pelianthus ii
somewhat laterally fused.

13. Corpuscles secreted at level below highest
point on style head = 0; corners of style head
secreting corpuscles somewhat above rest of

style head =

In all species of Stapelianthus the gynostegium
is perched upon a stipe, which is short in most but
up to 1 mm or more long in S. decaryi.

The outer corona lobes have a characteristic
shape that is unique to Stapelianthus: they are al-
ways broad and dorsiventrally flattened, erect above
the base and remaining close laterally so as to out-
line a deep cup in the base of which the inner lobes
are situated. In S. pilosus they are fused for nearly

Volume 91, Number 3 Bruyns & Klak 417
2004 Revision of Stapelianthus

Figure 2. Half-flowers in cy ieee ee —A. S. decaryi (PVB 5960). —B. S. pilosus (PVB 5959). —С. 5. insignis
(PVB 5957). Seale bar: A-C, 1 mm (at A). a = anther: e = corpuscle; са = calyx; co = corolla; 1 = inner corona
lobe: о = outer corona lobe; 5 = Spurs head: t = staminal tube.

half their length, while in all the others they аге velops in the middle of the back of each anther just
free nearly to the base. slightly above the level of the early stages of the

The inner corona lobes are short. incumbent on outer lobes. These give rise to the inner corona
the anthers, and do not usually exceed them. They lobes. Both series of lobes continue to grow, with
are joined by a ridge of tissue near their bases to the outer lobes spreading laterally as well so that

the outer series but have no dorsal horns or pro- eventually adjacent outer lobes nearly touch behind
jections. the inner lobes. The relative positions of the mature

The anthers are quadrate and horizontal to de- corona lobes of the two series can be seen in
scending but have sometimes been observed in S. Figure 2.

pilosus to possess a short, acute, apical appendage.
Fhe style head in Stapelianthus is somewhat соп- Pollinaria

cave above, as can be seen in Figure 2. Situated

between the anthers are five high points that are 14. Pollinia ellipsoidal = 0: D-shaped =

mostly well above the level of the center. though 15. Pollinia broader than long = 0: longer than
somewhat less so in S. pilosus than in the other broad —

species. It is on these high points that the corpus- 16. Pollinia with insertion crest exactly along edge
cles are secreted. Between these high points are = O: with insertion crest twisted onto dorsal
five lower areas into which the anthers are pressed. surface =

These lower areas are usually just below the level 17. Caudicle not widening toward apex = 0:
of the center of the style head. The anthers are then broader toward apex and somewhat spathulate
horizontal on top of the style head, with the inner beneath pollinium = J.

corona lobes descending toward the center. most

noticeably so in S. montagnacii and S. insignis. The In all species of Stapelianthus the pollinia are
outer edge of the five highest areas (between the longer than broad. In S. pilosus the pollinia are el-
anthers and bearing the corpuscles) slopes upward — lipsoidal and relatively small, with broad corpus-
so that the corpuscle is thus also held facing cles bearing small wings. In all other species of
obliquely inward, and this is true even in 5. pilosus. Stapelianthus the pollinia are larger and D-shaped,
The pollinia lie on the region sloping away from with the corpuscle widening toward the apex and
this highest area and also usually descend slightly flanked by long, narrow wings. The caudicle is usu-

toward the center. ally much broadened toward the top, with the pol-

The ontogeny of the staminal coronas has been linium attached to the broadest, rather spathulate
observed in Stapelianthus insignis. A small trans- part. In all species the insertion crest is attached
verse ridge first appears beneath each guide rail. on the edge at the top of the pollinium, after which
These ridges develop into the outer corona lobes. it twists around slightly onto the upper surface to-

At a slightly later stage a further small ridge de- мага the middle of the pollinium.

418

Annals of the
Missouri Botanical Garden

e 3.

5 in Stapelianthus. —A,
‚ В, S. decaryi (PVB 5 ж
bars: A. „ К, 2 mm n A); B

). F, " mm (at A). «
tubercle.

Seedlings

—
—
—

Hypocotyl uniformly colored = 0; mottled
= 1,
19. Cotyledon with + spathulate to elliptic blade-
l

let = 0; + without any blade =

Seed has been grown of Stapelianthus arenarius,
5. decaryi, S. insignis, S. montagnacii, and S. mad-
agascariensis. In all of them the hypocotyl is cune-
iform (Fig. 3) and mottled with purple on a pale,
creamy green background. The cotyledons are flat-
tened above, + deltoid, obtuse to acute, and, al-
though much reduced, are still distinguishable from
the hypocotyl. In 5
smooth,

. decaryi the whole surface is
the primary and secondary leaves are
paired, and for the first 2 to 4 nodes the stem is 4-
angled. In the others the surface is bullate, the up-
per surface of the cotyledonary tubercle is grooved
toward the base, and for the first few nodes the stem
is 4-angled. In S. arenarius the primary stem grad-
ually bends toward the surface of the soil to assume
a + prostrate habit. This happens before the side
branches develop.

RESULTS

Sequence length in the chloroplast trnL-trnF re-
gion varied between 835 and 889 bp with the ma-
jority of species measuring 855 bp. Numerous in-
dels were present in the trnL-trnF gene region. In
this study all gaps were treated as single sites re-

Whole plantlet after + 3 weeks.
. D, s madagascariensis (PVB 5958). К.
= cotyledon; h =

B, D. F. C 5 ot apex of
F, S. arenarius (PVB 5954). Scale
hypocotyl; p = primary leaf ыш nt and

gardless of their length and were coded as binary
characters to be added to the data matrix and in-
cluded in the analyses. The longest insertion (17
bp) was recorded for Duvalia maculata, whereas
the longest deletion (10 bp) was found in Duvalia
sulcata. One indel was found to be parsimony in-
formative.

The nuclear ITS] region varied between 575 and
578 bp in length. Several species had single indels,
and Orbea ubomboensis had an insertion of 3 bp.
There were no informative indels.

Statistics, including numbers of variable posi-
tions and measures of consistency, are given for
each analysis in Table 2. There were no areas of
ambiguity in the alignment (available from the au-
thors)

trni-trnY ANALYSIS

The strict consensus (not shown) of the 19 trees
recovered (L = 20, CI = 0.700, RI = 0.885, RC
= 0.619) shows a monophyletic Stapelianthus
(ackknife (JK) = 62) but without resolution among
the species. Sister to Stapelianthus are the repre-
sentatives of Ballyanthus, Duvalia, Huernia, Orbea,
Tavaresia, and Tridentea. These, together with Sta-
pelianthus, form a strongly supported but unre-
solved monophyletic group (ЈК = 81). Baynesia is
the sister to this entire clade (JK = 90). Only 13
informative characters were found, including one
indel.

Volume 91, Number 3 Bruyns & Klak 419
2004 Revision of Stapelianthus

—
—

Table 2. Summary of statistics for parsimony analyses of Stapelianthus and related taxa. СІ = Consistency Index,
= Retention Index, RC = Rescaled Consistency Index.

Vari- Inform-

Total able ative
char- char- char- ee No. о
Analysis acters Indels acters acters length trees Cl RI RC
trnL-trnF 889 l 38 13 20 19 0.700 0.885 0.619
TS 578 — 69 35 62 28 0.677 0.823 0.558
Morphology 19 — 19 19 13 1358 0.442 0.788 0.348
Combined 1: trnL-trnk & ITSI 1407 | 107 18 85 5 0.659 0.824 0.543
Combined 2: trnl.-t
ITS] & M аш 1486 1 107 67 144 84 0.521 0.752 0.392

ITS] ANALYSIS 66). Sister to Stapelianthus are the representatives of

m . Ballvanthus, Duvalia, Duvaliandra, Huernia, Orbea,
The strict consensus 2 may of p 28 trees -

— арт Сї = RE = 0.823. RC and Tidenten (le., similar to the results of the trnl -
= 0.558) shows а highly иш: Miis э unf analysis) a clade of support with JK = 4.
Stapelianthus (JK = 98) but with low resolution МЕЈ 19 informative characters ее found. |
among the species. All the remaining stapeliads Combined analysis I (tmL-tmF and ITS genic
sampled are arranged in a polytomy of which Sta- regions). The strict consensus (Fig. 4) of the five
pelianthus is the largest and best-supported clade, trees recovered (L = 85, CI = 0.059, RI = 0.824,
V RC = 0.543) shows a well-resolved, and in many

Morphological analysis. The strict consensus parts also well-supported, phylogeny. Stapelianthus
. is monophyletic (JK = 100) in which S. insignis.
= 0.442. RI = 0.788. RC = 0. 348) shows a weakly S. madagascariensis, and 5. montagnacii form a
supported and internally unresolved clade made up poorly supported clade (ЈК = 62). Sister to Stape-
of all species of Stapelianthus and Tavaresia (JK = — lianthus is an unsupported clade made up of the

(not shown) of the 1358 trees recovered (L =

C

Table 3. Character states for the 19 morphological characters used in cladistic analysis.

Characters
Species 1-5 6-10 11-15 16-19
Riocreuxia flanaganii 02000 00100 00000 0000
Ballyanthus prognathus 00010 00011 01001 0127
Baynesia lophophora 00100 00100 00000 0000
Caralluma crenulata )0( 01020 0000? 0000
Duvalia mac 1 8 11011 01001 0101
Duvalia at 11011 01001 0101
л, dioscoridis 00011 21010 02001 01??
Echidnopsis malum 1000 00100 1100? 0000
Huernia verekeri subsp. pauciflora 11011 11001 01001 0101
Orbea araysiana 00011 00010 00011 1101
Orbea ubomboensis 00010 00010 00011 1101
iytidocaulon ciliatum 00100 00000 00000 0000
Stapelianthus arenarius 10111 11000 10111 1111
Stapelianthus decaryi 01011 11100 LOLLI 1111
Stapelianthus insignis 10111 11110 10113 UL
Stapelianthus keraudreniae 10111 11010 LOTTI 22:33
Stapelianthus madagascariensts 10111 11100 10111 ae Bak
Stapelianthus montagnacti 10111 11100 10111 paa a
Stapelianthus pilosus 01011 11200 11101 1977
Tavaresia barklyi 01011 11100 10111 1101
Tridentea peculiaris 00001 11010 00011 1100

420 Annals of the

Missouri Botanical Garden

Stapelianthus madagascariensis

Stapelianthus montagnacii

EN

Stapelianthus insignis

100 Stapelianthus decaryi

Stapelianthus pilosus

Stapelianthus keraudreniae

Stapelianthus arenarius

Tavaresia barklyi
Orbea araysiana
Orbea ubomboensis
Tridentea peculiaris

Ballyanthus prognathus
66
Duvalia sulcata
Duvalia maculata
86

98

Baynesia lophophora

Huernia verekeri
Duvaliandra dioscoridis

Echidnopsis malum

Rhytidocaulon ciliatum

zi

Caralluma crenulata

Riocreuxia flanaganii

Figure Strict consensus tree of five trees obtained from combined analysis of trnL-trnF and ITS] data (L = 85,
Cl = 0.6! 59, RI = 0.824, and RC = 0.543). Numbers above branches indicate supporting jackknife percentages, where
e are above 50%.

representatives of Ballyanthus, Duvalia, Huernia,
Orbea, Tavaresia, and Tridentea, so that no close
relatives of Stapelianthus appear to be among these
taxa. The phylogram based on one of the five trees
(Fig. 5) shows an especially long branch at the base

of Stapelianthus, which again suggests that it is
very distinct from the other African taxa.
Combined analysis 2 (trnL-trnF, ITS genic re-
gions, and morphology). The strict consensus
(Fig. 6) of the 84 trees recovered (L = 144, CI =

Volume 91, Number 3
2004

Bruyns & Klak
Revision of Stapelianthus

Duvaliandra dioscondis

Caralluma crenulata

Riocreuxia flanaganii

— 1 change

Echidnopsis malum

Stapelianthus madagascariensis
Stapelianthus montagnacii
Stapelianthus insignis
Stapelianthus decaryi
Stapelianthus keraudreniae

Stapelianthus pilosus

Stapelianthus arenarius

Tavaresia barklyi

Orbea araysiana

Orbea ubomboensis

Tridentea peculiaris

Ballyanthus prognathus
Duvalia sulcata
Duvalia maculata

Huernia verekeri

Baynesia lophophora

Rhytidocaulon ciliatum

ure 5. Phylogram based on one of five trees obtained from combined analysis of trnL-trnF and ITS1 data. The

Fi g
le ae of the branches are drawn in proportion to the number of character changes

0.392) shows again a
100). Within it
there is a clade consisting of S. arenarius, S. insig-
nis, S. keraudreniae, S. madagascariensis. and 5.
= 7A) to which the remaining two

0.521, RI = 0.752, RC =
well-supported Stapelianthus (JK =

montagnacti (JK

species are sisters. Tavaresia resolves here as a sis-
ter to Stapelianthus but with very weak support (JK
= 56). whereas based on molecular characters
alone (combined analysis 1) it was sister to Orbea

araysiana (JK — 92).

422 Annals of the
Missouri Botanical Garden

100

56

Stapelianthus madagascariensis
Stapelianthus montagnacii

Stapelianthus insignis

— — Stapelianthus keraudreniae

Stapelianthus arenarius

Stapelianthus decaryi

Stapelianthus pilosus

Tavaresia barklyi

Orbea araysiana

96

Ballyanthus prognathus

Duvalia maculata

Huernia verekeri

Duvalia sulcata

Tridentea peculiaris

Orbea ubomboensis

Baynesia lophophora

Duvaliandra dioscoridis

—

Echidnopsis malum
92 |

o LLL Rhytidocaulon ciliatum

Caralluma crenulata

Figure 6. eis O tree of 84. trees Үрү [гот
| =

data (L = 144, CI = 0.521, RI = 0.752, and RC ).392).

DISCUSSION

Our morphological survey outlines the wide var-
iation that is found in most features of members
of Stapelianthus. It has shown that the defining
characteristics of Stapelianthus are the spineless

Riocreuxia flanaganii
combined analysis of traL-trnF, 1751, and morphological
Numbers above branches indicate jackknife percentages.

stems combined with the ascending to erect, deep-
ly bifid outer corona lobes, which form a cup
around the top of the gynostegium containing en-
tirely the small and horizontal to slightly descend-

ing inner lobes.

Volume 91, Number 3
2004

Bruyns & Klak 423

Revision of Stapelianthus

|. PHYLOGENETIC. RELATIONSHIPS

Morphological evidence. In the morphological
analysis (not shown) Tavaresia becomes part of the
Stapelianthus clade (although weakly supported, JK

66). One might hesitate at this conclusion, es-
pecially because of the unusual leaf rudiments of
Tavaresia. While the leaf rudiments of many Sta-
pelianthus bear some resemblance to those of Huer-
nia, those of Tavaresia appear to be very different.
However, the epidermal cells on the filiform leaf
rudiments of 5. pilosus are similar to those observed
on young leaf rudiments of Tavaresia (and also doc-
umented for Hoodia in Bruyns, 1993, fig. 4D, F).
They seem to represent a transitional stage from
normal epidermal cells to the elongated ones found
on all stapeliad spines (including those of Tarare-
sia). They are, in fact, rather dissimilar to those on
the filiform leaf rudiments of Huernia pillansii,
which is the species of Huernia bearing the greatest
vegetative similarity to 5. pilosus. The pair of spines
al the base of each main spine in Zavaresta are nol
stipules (Meve & Albers, 1990) and should possi-
bly be interpreted as an extreme form of the hastate
leaves found in some forms of Ceropegia linearis H.
Mey. or in Microloma sagittatum (IL) R. Br., a ran-
dom phenomenon in various unrelated groups,
which is probably of little taxonomic significance
at higher levels. It may be added that the flower of
Stapelianthus decaryi also has a similar shape and
papillate surface inside to the flower in Tavaresta.

In assessing the validity of this result, five fur-
ther characters deserve mention. (Here the genera
Duvalia, Huernia, Orbea, Stapelianthus, and Tava-

resia are all brought into consideration.)

(1) Outer corona

In Huernia the outer corona descends from its
point of attachment to the staminal column toward
the base of the corolla, while in Duvalia it remains
more or less horizontal: at any rate in both it keeps
entirely away from the remainder of the gynoste-
gium. This is different from the position in Orbea,
Stapelianthus, and Tavaresia.

The cup formed by the outer corona in Tararesta
is fused toward the base into a single structure and
the same is true in Stapelianthus pilosus. However.
in Tavaresia, in early stages the outer corona con-
sists of five discrete lobes and fusion takes place
only later. In these early stages it is impossible to
separate gynostegia of Tararesia and. for example,
S. insignis. The position in Orbea is more variable
and was dealt with in detail in Bruyns (2002).

(2) Inner and outer guide rails

The presence of inner and outer guide rails in
Huernia was first noted by Kunze (1982), and he
of the Marsden-
ieae). They are also present in Duralia. In Huernia

—

observed this also in Stephanotis

the guide rails are seated on rather inflated cush-
ions. These are absent in Duvalia, where the space
behind the outer guide rail is much reduced. Fur-
ther reduction is found in Orbea, Tavaresia, and

Stapelianthus.

(3) Position of insertion crest on the pollinium

The position of the insertion crest along the edge
of the pollinium in Duvalia and Huernia means
that, once inserted, the pollinium lies with its flatter
surface parallel to a radius from the center of the
flower. and there must be sufficient room between
the guide rail and the outer corona series for this
to take place. This arrangement is found in several
venera of the Ceropegieae (Bruyns, 2000). In the
Marsdenieae, Hoya species with an insertion crest
always have it exactly along the edge.

The condition in Orbea, Stapelianthus, and Ta-
varesia, where the insertion crest lies partly on the
upper surface means that, on insertion, the pollin-
ium will lie with its upper (flattish) surface partly
turned toward the center of the flower. This allows
for the development of much larger pollinia than in
Duvalia and Huernia, but also for much greater re-
striction of the space between the outer corona and
the guide rails and thus for greater involvement of
the outer corona in guiding insects into the correct
position for pollination. This arrangement is unique
to the Ceropegieae, where the outer corona is also
more developed than in any other tribe.

(4) Shape of the pollinia

The shape of the pollinia in Orbea. Stapelian-
thus, and Tavaresia is very similar and is somewhat
different from that in Duralia and Huernia.

It will usually be found that, while pollinia in
Duvalia and Huernia thicken uniformly toward
their center (i.e., they are more or less ellipsoidal),
in Orbea. Stapelianthus, and Tavaresia they are
thickest toward the curved part of the “D” and are
significantly flattened toward the insertion crest. In
this respect the pollinia of S. pilosus are rather un-
usual, and they show some similarity to "typical"
Huernia pollinia.

(5) Shape of the top of the style head

The peculiar concave shape of the style head in
Stapelianthus and Tavaresia reaches an extreme in

424

Annals of the
Missouri Botanical Garden

Tavaresia, where it is unusually thin at the center

(Bruyns & Forster, 1991: fig. 7B). It is never quite
as thin in Stapelianthus or in any other species,
such as Orbea maculata (Bruyns, 2002).
such a construction is found.

where

—

An oddity of this con—
struction is the manner in which the parts that se-
crete the corpuscle may extend far above the level
of the rest of the style head. Observations of early
stages of the flower indicate that this is a late de-
velopment, and it causes both the exposed situation
of the corpuscle, the peculiar, nearly horizontal ori-
entation of the guide rails, and the situation in some
cases where the pollinia actually descend in the
anther thecae.

Therefore, there are several morphological fea-
tures that suggest an alliance of Stapelianthus with
Tavaresia.

4, 5).

analyses of the two molecular data sets (not shown)

Molecular evidence (Figs. The separate
both show Stapelianthus as a monophyletic clade.
The relationship of Stapelianthus with Tavaresia,
deduced from the morphological evidence, is not
supported by the molecular data, where Tavaresia
is most closely related to Orbea araysiana (JK

82). In the molecular analysis Ballyanthus, Duva-
Orbea,

shown to be the most closely related genera to Sta-

lia, Huernia, Tridentea, and Tavaresia are
pelianthus among the taxa selected for the study (JK
= 88). However, no well-supported close relation-
ship of Stapelianthus to any of these genera was
retrieved.

The evidence from the 48 informative purely mo-
lecular characters is that Stapelianthus occupies a
distinct evolutionary line and that it is not espe-
cially closely allied to any of the African stapeliads.
The relatively isolated position of Stapelianthus
from the rest of the study group is particularly ev-
ident in the phylogram (Fig. 5) and is indicated by
the long branch subtending the Stapelianthus clade.
The many changes of characters at the base of this
clade may also suggest that the genus has been
isolated from the remaining taxa for a long time.

Infrageneric relationships are both poorly re-
solved and poorly supported. Only Stapelianthus in-
signis, 5. madagascariensis, and 5. montagnacii are
resolved as a weakly supported clade (JK = 62)
within the genus.

Combined morphological and molecular evidence
(Fig. 6). When

characters are added to the two sets of molecular

the 19 informative morphological

data, a weakly supported sister relationship be-
tween Stapelianthus and Tavaresia is formed.
Here infrageneric relationships remain both
poorly resolved and poorly supported, and one finds
that S. decaryi and S. pilosus are sister to the re-

This reflects

14).

the fact that morphologically S. arenarius, S. insig-

mainder of Stapelianthus (JK

nis, 5. keraudreniae, S. madagascariensis, and 5.
montagnacil are all quite similar, while S. decaryi
and S. pilosus are more distinctive, with S. pilosus
by far the most distinctive. In fact, S. pilosus has
so many autapomorphies (such as the cylindrical,
uniformly colored stems, the conical tubercles, and
the slender leaf rudiments) that it could be said to
be immediately recognizable among all of the 320
or so species of stapeliads, whether it is in flower
or not. It is interesting that this is not corroborated
by the molecular characters, where there is re-
markably little variation among all the species of
Stapelianthus and especially between such appar-
ently distinctive species as S. pilosus and S. aren-
arius, as the phylogram (Fig. 5) demonstrates. This
suggests that, whereas the genus may have been
isolated for a considerable time, the few changes in
molecular characters that were detected among the
species may point to a more recent radiation of the
species within Madagascar.

2. BIOGEOGRAPHY AND ECOLOGY

Stapelianthus is endemic to Madagascar and is
the only stapeliad genus found there. The seven
species grow only in the extreme south and south-
west of the island from Fort Dauphin in the east to
Morombe in the west (Fig. 7). These are the driest
parts of Madagascar, typically receiving less than
400 mm of rain annually, though it appears that the
rainfall west of Fort Dauphin (where S. decaryi oc-
curs) may exceed 1000 mm in a year.

The most widely distributed species is Stapelian-
thus decaryi. This is found from near Fort Dauphin
in the east northward to Ihosy and Zazafotsy on the
southern edge of the central plateau and westward
to Ambovombe.

The next most widely distributed species seem
to be Stapelianthus insignis and S. madagascarien-
sis. Stapelianthus insignis occurs from Tulear at
least as far as Ejeda, Itampolo, and Ampanihy
(Rauh, 1993: 36) and 5. madagascariensis from Tu-
lear to Ambovombe: of these two, the latter is prob-
ably the more widely distributed. Stapelianthus pi-
losus and S. keraudreniae appear to be rather local:
and
Behara in the south and 5. keraudreniae around

the former between Ambovombe, Tsihombe.

Betioky in the southwest. Stapelianthus montag-
nacu occurs from Morombe southward for at least
50 km but might also occur north of Morombe,
since the woodland dominated by Didierea mada-
gascariensis Baillon, with which it is associated, ex-
tends northward to just south of Morondava (Rauh.

Volume 91, Number 3
2004

Bruyns & Klak 425

Revision of Stapelianthus

45° 50°E
|

Figure 7. Distribution of Stapelianthus.

1978: 11). The distribution of S. arenarius is poorly

known.

The only records of species occurring together

are of Stapelianthus madagascariensis and S. pilo-

sus around Tsihombe ii

—

the island.

It would appear that most of the species are hab-
itat-specific, and this is especially true of. Stape-
lianthus arenarius and S. insignis in the west of the
island and of S. decaryi, which is the only species
to be found on gneiss domes. It could well be.
therefore. that edaphic factors have been an im-
portant driving force behind speciation in Stape-
lianthus.

TAXONOMY

Stapelianthus Choux, in A. C. White & B. Sloane,
l: 71. 1933. TYPE:

madagascariensis (Choux) Choux.

Stap.. ed. Stapelianthus

the southernmost part of

Stape liopsis Choux, 2 Rend. Hebd. Séances Acad.
Sei. Paris | э 444. n. illeg.,

nom. non Stape-

ops African Gard. 28: 32. 928. nec
Supp p lips. FI. Py South Mrica: t. 445.
19

PYPE: Stapeliopsis madagascariensis C houx.

Small spineless non-rhizomatous succulent,
forming dense to diffuse mats up to | diam.:
stems 25-200(-400) mm long, 3-15 mm thick, pro-
cumbent to decumbent, fleshy and firm, glabrous:
tubercles arranged into 4 to 8 angles or densely cov-
ering the stem, not laterally flattened, each bearing
a small leaf rudiment, which soon dries out and

falls off. often bullate, without stipular denticles.

=.

Inflorescence glabrous, 1 per stem near base, о
to 3(5) flowers developing in slow succession from
peduncle < 2 mm long. with 1 to 3 deltoid bracts
< 1 mm long without lateral teeth: pedicel 3-12
mm long. 1-2 mm thick, ascending: sepals 2.0-9.0
mm long, subulate to lanceolate, acute. Corolla 10—
35 mm diam., rotate to cylindrical sometimes with

prominent shiny annulus; outside glabrous and
smooth: inside usually with many conspicuous су-
lindrical obtuse papillae (very small and few only
in S. insignis), each with a small apical bristle: tube
usually just containing gynostegium: /obes usually
deltoid,

folded into spreading often acute lobule. margins

spreading, + with tissue between them

eciliate: corona 2.0-6.5 mm tall, 4-8 mm broad.
consisting of two series arising on staminal tube
and partly intergrown, glabrous, very dark red or
purple: outer lobes 2.5—7.5 mm long, mostly erect
from base and spreading toward tips (rarely spread-
ing from base, $. arenarius), free usually practically
to base. forming cupular structure around central
part of gynostegium and mostly much exceeding
this. dorsiventrally flattened, deeply to shallowly bi-
fid into erect to somewhat recurved narrowly deltoid
lobules; inner lobes 0.4—1.0 mm long, adpressed to
backs of anthers and rarely exceeding them, dor-
siventrally flattened, small and inconspicuous, dor-
sally fused to cup formed by outer corona lobes:
anthers horizontal to. descending on top of style
head, margins shrinking back to expose pollinia,
rectangular: pollinium D-shaped, insertion crest
twisting from outer edge to dorsal surface, caudicle
attached with broad cupular pad to base. Follicles
erect, terete-fusiform, obclavate, slender, consisting
of 2 horns diverging at 30-1505, longitudinally mot-
tled with narrow broken purple stripes, glabrous
and sometimes rugulose; seed + flat with cream,
foam-like border and the rest pale + brown,

KEY TO THE SPECIES OF STAPELIANTHUS IN MADAGASCAR

la. Stems densely covered with small conical tuber-

426

Annals of the
Missouri Botanical Garden

cles, each em with a fine recurved hair-like
leaf rudimer S. pilosus

. Stems dieting tly 4—6(—8)-angled, tubercle tipper ed
with a conical to narrowly deltoic

—
—
~

leaf rudiment.

2a. Corolla with cylindric al tube; stems s decunie
bent to erect with smooth surfac
I. S. i disi
2b. Corolla tube not cylindric ini: stems procum-

bent with bullate surfac
3a. Corolla + rotate.
4a. Corolla with conspicuous shiny an-
to dull vel-
low spotted with wine- to purple-red
on lobes 1. S. keraudreniae
Corolla without annulus, le
white with red-brown spots

nulus, inside greenish

4b.

insic

ы
т

> | 3. S. arenarius
Corolla shallowly campanulate or bi

ag ook late.
a. Corolla

bicampanulate, | inside
smooth except for few m ae
ae along edges of lobe

5. A insignis
5b. 1 shallowly campanulate. in-
side covered with
sle id `r papillae
Oa.

conspicuous

Corolla inside maroon to red on
lobes mottled with cream in
tube, outer corona lobes bifid
in upper third only

C
T

S. l
Corolla та cream with ma-
гооп spots, outer corona bifid

at least to mi 80

6b.

EA E EE ariensis

1. Stapelianthus decaryi Choux, Ann. Inst. Bot.-
Géol. Colon. Marseille ser. 5, 2(3): 7. 1934.
TYPE: Southern Madagascar. Near Anosy,
gneiss rocks on the eastern shore of the Ran-
ofotsy Lagoon, July 1932, R. Decary s.n. (miss-
ing) (lectotype, selected here, Choux (1934:
Planche IID)). Figure 8.

Stems (10—)25—100 mm long, 5-15 mm thick,
forming dense clumps, decumbent to erect, gray-
green to brown mottled with dark brown, surface +
smooth; tubercles flattened-conical, weakly joined
into roughly 6(to 8) angles up stem, tapering
abruptly into a narrowly conical spreading leaf ru-
diment 2-4 mm long and < 1 mm broad, which
soon withers but persists for a time as a white near-
ly spine-like husk. Pedicel 4.0-8.5 mm long, 1.5-
2.0 mm broad, ascending, holding flower facing up-
ward; sepals 3-6(—7) mm long, 1.5-2.0 mm broad
at base, ovate-lanceolate, acuminate, with narrow
sometimes slightly recurved tips, green to cream.
Corolla (10-)15-23 mm diam., tubular-campanu-
late; outside cream with fine round maroon spots;
inside densely covered in upper half of tube and
on lobes (becoming sparser and smaller in lower
third of tube) with cylindrical papillae up to 0.6

mm long (usually with red to blackish apex) each
tipped with an ascending bristle, cream with fine
maroon spots usually becoming uniformly maroon
on lower half of tube; tube (5—)10—16 mm long, б—
9 mm broad, cylindrical, usually narrowing slightly
toward mouth and widest near base; lobes 5.0-8.5
mm long, 4—8 mm broad at base, deltoid, acute to
acuminate, spreading to reflexed; corona 5.0-6.5
mm tall, 4—6 mm broad, dark maroon, raised on
white (with few purple-red spots) pentagonal stipe
up to 1.5 mm long; outer lobes 4.5—6.0 mm long,
erect to slightly spreading, divided to middle or be-
low into slender almost filiform slightly diverging
to erect teeth, sometimes with a further small tooth
between them; inner lobes + 0.6 mm long, deltoid

obtuse, but not usually exceeding anthers. Follicles
fusiform, erect, diverging at 20-30° from one an-
other, surface smooth and mottled with longitudinal
purple lines on a cream background; seed variable
in size, 5.0-6.0 X 2.54.0 mm. elliptic to nearly

circular, border rather inflated, whole seed pale
brown or yellow-brown.
Distribution. Widely distributed in southern

Madagascar. Elevation 10-900 m.

Ecology. Stapelianthus decaryi mainly inhabits
pockets of soil or leaf litter on gneiss domes along
the foot and lower slopes of hills. Plants are gen-
erally found growing entirely in the open, without
any protection. Around Fort Dauphin it is common
and grows in the company mainly of Pachypodium
horombense H. Poiss., Kalanchoe orgyalis Bak., and
Ischnolepis graminifolia (Costantin & Gallaud)
Klack. Around Ihosy the habitat is very similar, and
here it grows with Pachypodium rosulatum, Kalan-
choe orgyalis, and Euphorbia xylophylloides A.
Brogn. ex Lem. among a host of other succulents.
Near Zazafotsy it was observed on flat, gneiss out-
crops covered scantily with Xerophyta, Aloe inter-
media (H. Perr.) Reynolds, and Kalanchoe synse-
pala Bak.

Discussion. Stapelianthus decaryi is most easily
recognized when sterile by its almost erect stems
clustered together into densely packed clumps
(which may be up to 1 m diam.) with their almost
spine-like leaf rudiments. The tubular flowers cov-
ered densely inside with short, conical papillae are
also distinctive. The flowers are extremely variable,
and some with tubes as short as 5 mm were ob-
served near Ihosy.

In Stapelianthus decaryi several follicles have
been seen, and they have been found to contain
variable numbers of seeds: 35 seeds were counted
in one solitary follicle, 76 in another pair, 52 in
another pair, and 12 in a further very small pair.

Volume 91, Number 3 Bruyns & Kla 427
2004 Revision of e M

AC

y SUPE
MAN a ah ASN

a 7 NA
ET a
A a лл *
a a *
D т»

>
Ie

Figure 8. SOMME 2 8 5 —А. Eus of stem. —B. Leaf rudiment. —C, D. Side view of flower. —E. side
view al dissected flower . Side view of gynostegium with tall basal stipe. —G. Side view of gynostegium with one
outer corona lobe re moved a with muc т ae stipe. v 'apillae inside corolla eee mouth of tube. —l.
eng = ale bars: A, C-E, 3 mm (at E); B. 1 mm: F, G, | mm (at F); H. 0.5 mm (at F); J. 0.25 mm (at F). Drawn
from A-C, ». hort. p Boer; D. Н, hort. dafs E eee

The type of Stapelianthus decaryi is missing. One zofoty. 6 Fe a 1989, Du Puy et al. 19877 (TAN): Ando-
` hahela, Parcelle 2, 125 m, Phillipson 2922 (K, P); near
| . . Italy, Descoings 2669 (P), Du Puy et al. M 838 (К); Ber-
selected as a lectotype, since this clearly illustrates ente Reserve. Lucille 948 (P): Ranopiso, Decary 10721
both the shape and habit of the stems and the shape (Pj; near Ihosy, Bosser 19684 (P); Andrahomana. Decar)
of the corolla and thus characterizes the species 3114 (P).

of the illustrations published with the protologue is

clearly.
Sp ecimens examined. MADAGASCAR. N of Zazafot- 2 Stape ‘lianthus pilosus Lavranos & D. S. Har-
‚ Bruyns 6191 (BOL); Zazafotsy escarpment, 22 July dy, J. S. African Bot. 27: 237. 1961. Tricho-
1958. Descoings Een (TAN); Fort Dauphin, Daing: caulon Fee Choux. Ann. Inst. Bot.-Géol.
3759 (TAN): 8 km W of Ihosy, Bruyns 6216 (BOL): valley Calon; Marseille ser: d ) 1932
of Manambolo, near Toman 400-900 m, Dec. 1933 E dl s | HN M
Humbert 13160 (P); 50 km W ч Fort Dauphin, Horde ГҮРЕ: 5ошһегп Madagasc - Mount Angayo;
RE); e 9 Jan. 1033. Decary (К. TAN): l Apr. 1931, А. Decary 8820 (lectotype, se-

Manambaro, Bruyns 5960 (BOL); Abe near Ha- lected here, Pl: isotypes, RI, TAN!). Figure 9.

428

Annals of the
Missouri Botanical Garden

E a A ER:

14,
d P Why
` JR

- LM
WC VN e
E JJ

Figure 9,

E. Side view o ected flower. —F. Face
gynostegium with one outer corona lobe removed. =Í.
Scale bars: A, 1 mm; B, E, 2 mm (at B); C. D, 3 mm m ا‎ C);

Drawn from A, D, I, J, PVB 5959. rest, hort. de Boe

Stems 30—300 mm long, 8—12 mm thick, decum-
bent (rarely procumbent), green (purplish when ex-

posed), smooth, ^ cylindrical, covered densely with

conical tubercles each tipped with a filiform leaf

rudiment 2.5-6.0 mm long. leaf rudiment rapidly
drying out to a persistent recurved whitish hair.
Pedicel 3—7 mm long, 1.0-1.5 mm thick, ascend-
ing, holding flower facing at least partly upward,
green sometimes speckled with purple and some-
times with scattered. papillae toward apex; sepals
3.0-4.5 mm long, 1.0-1.5(—2) mm broad at base.
subulate, acuminate-filiform usually curling back-
ward toward apex, green sometimes speckled with
purple, smooth. Corolla 10—18 mm diam., campan-
ulate; outside cream spotted with maroon: inside
covered with slender columnar papillae 0.50—0.75
mm long each with a sharp apical bristle, cream to
pale yellow spotted with dark purple: tube 3—4 mm
long, cupular; lobes 3.5-7.0 mm long, 4-6(-97) mm
broad at base, deltoid, usually spreading with api-
ces somewhat recurved; corona 3.54.0 mm tall,
2.5-3.0 mm broad,

dark maroon, seated on short

vids oe pilosus. —A. Tubercles on stem. —B. Face view of flower. —€
dis view of gynostegium. —G. Side view

d 0 e ar near base of lobes. —J.

А |
АІ) f

XI M/ /
HA £
VE M,
* А |

„ D. Side view of flower.

Side view of
Pollinarium.
, | mm (at C); J. 0.5 mm (at C ); J. 0.25 mm (at €

ol g поче. —Н.

—

stipe: outer lobes 2.4—3.5 mm long, fused for nearly
half length of gynostegium, erect with spreading
apices, convex outside and somewhat concave with-
in, deeply bifid into + parallel narrowly lanceolate
acute lobules; inner lobes + 0.4 mm long, deltoid,
obtuse, usually not exceeding anthers.

Distribution. Southern Madagascar, between
Tulear and Behara. Elevation 1-500 m.

Ecology.

small bushes in denuded areas or even in exposed

Stapelianthus pilosus may grow among

places on rocks. However, it appears to prefer dry,
xerophytic forests, where plants thrive in accumu-
lations of leaf litter on the floor of the forest.
Discussion. Choux described this as Trichocau-
lon decaryi because of its very unusual stems.
Within Stapelianthus, where the inflorescence,
flowers, and especially the corona suggest it be-
longs, it occupies a rather isolated position mor-
phologically. In the other species of the genus the
surface of the stem is bullate, marked with dark
patches on a pale background: here it is smooth

Volume 91, Number 3
2004

Bruyns & Klak 429

Revision of Stapelianthus

Figure 10.
gynostegium with part

A, 3 mm; B, C. | mm He m D, 0.5 mm (at БВ); F

and uniformly green (if sheltered). The sepals are

unusually long and slender relative to the size of

the flower. The corona is also unusual in that the

outer lobes are fused into a cup to just below their

middle. The pollinaria are particularly small with
a disproportionately large corpuscle, nearly ellip-
soidal pollinia, and short wings on the corpuscle.

Material at P indicates that Decary discovered
this species al Mount Kokomba in January of 1918
Choux (1932: 10) provided a Latin diagnosis of this
n cies but did not mention a type specimen with

. However, on page 6 he mentioned two collec-
tions, namely Decary 8820 from Mount Angavo and
Decary 9033 from between Behara and Tranomaro.
Decary 8820 is at K. P. and TAN,
9033 has only been located at BM. Since it is more
widely distributed, I have selected Decary 8820 as
the lectotype.

Angavo, Rauh

Specimens examined. MADAGASCAR
9162 (PRE). Decary 4549 (PRE); between Behara and
Tranomaro, e ary 9035 (BM); 12 % N of Be а ris
2936 (PRE): Mt. Kokomba. 180 . Decary s.n. [Si-
hombe, е p^ 59 (BO "i pæ ed N of Behara, т. Ps
& Supthut BVA 30 (TAN); N side x s Estuary, 1—
150 m, Humbert & 1 29541

=

3. Stapelianthus arenarius Bosser & Morat. Ad-
340-341. 1971. TYPE:
Western Madagascar. Route to Manombo N of
Tulear, J. Bosser & P. Morat 20392 (holotype,
P not seen). Figure LO.

ansonia RUM

pu 5 е Bull. Mus. Nall. Hist.

В, Adansonia, 12: 990. Syn. nov. TYP

oa стн аг. 1 8 2 Apr. 1972, P. Morat
3973 (holotype, P not seen).

=
c
=
=

5 arenarius.—A. Face view of flower. —
corolla tube. —D. P: sae inside 2 near base of lobe
|. 0.25 mm (at B).

while Decary

. Face у view of

ле w of кюч —C. Side
—E. Pollinarium. Scale bars:

Drawn from PY "E

Stems 50-150 mm long, 5-10 mm thick, pro-
cumbent often with apices ascending, gray-green
marked with purple-brown, surface bullate: tuber-
cles arranged roughly into 4 rows, tipped with a
small narrowly lanceolate recurved leaf rudiment
1-2 mm long and 0.5 mm broad, slightly flattened
above. Pedicels 3-10 mm long. 1.0-1.5 mm thick.
erect, holding flower facing upward, pinkish green;
1.5 mm broad at base.

sepals 2.0—4.0 mm long.

lanceolate-acute, whitish. Corolla 20-25 mm diam.,
+ rotate: outside dull white finely dotted with pale
maroon; inside finely papillate over whole surface
except base (papillae up to 0.3 mm tall). white with
few maroon spots toward base. tube white spotted
tube + 2

mm deep, very broad and shallow, containing gy-

with maroon coalescing behind corona:
nostegium: lobes 8-13 mm long, 4.5-5.5 mm broad
at base, deltoid-acute, spreading to recurved; co-
гопа 2 mm tall, 4-5 mm broad, maroon-black, seat-
ed on very short stipe: outer lobes 2.5-2.8 mm tall,
free practically to base, bifid to below level of inner
lobes into slightly ascending-spreading narrowly
inner lobes 0.7—1.0 mm long, linear
Fol-

licles fusiform, with fairly slender horns (3—4 mm

obtuse teeth;
oblong, + adpressed to and equaling anthers.

thick at max.) diverging at + 150°, surface covered
with irregular ridges and mottled with purple on a
paler background; seed 6.9-6.5 X 3.0 mm, pear-
shaped, slightly raised pale border, rest pale pink-
ish brown.

Distribution. Southwestern Madagascar. Eleva-
tion 10-100 m

Ecology. Stapelianthus arenarius grows in fine,

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Annals of the
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Figure |
flower. —D. Side view of gynostegium with one outer corona pes remov
of lobes. —F. Pollinarium. Se ale bars: A-C, 3 mm (at В);

hort. J. Н. v. d. Merwe.

deep, red sand within 1 km of the sea in Didierea

madagascariensis forest north of Tulear, where
plants are common among leaf litter under bushes
and trees. Their wrinkled surface lends them an

extraordinary resemblance dried twigs: when
very dry they become prostrate and partly hidden
8 dried leaves and practically invisible, when
in better condition rising up out of the leaf-litter
са becoming much more visible.

Discussion,
they are nearly flat with white corolla lobes (some-

This species has unusual flowers:

times faintly brownish) becoming spotted with ma-
roon toward the center. The stems are paler, much
more rugulose than those of other Stapelianthus
species, with very slender leaves, and they are not
clearly 4-angled especially when in a dry state. The
rugose follicles are unique in the genus and among
all the stapeliads.
There seem to be no obvious reasons not to in-
clude Stapelianthus calcarophilus under S. arenar-
In S. calcarophilus the sepals and flowers are
slightly smaller and the corolla lobes are reflexed.
These differences are minor indeed and seem to be
outweighed by the similarity between them in the
shape of the flower and its coloring as well as in
the shape and also the orientation of the outer co-

l. Sta ^ii d keraudreniae.—A. Portion of stem. —B. ii ‘e view of flower.
I
Р

view of dissected

—C. Side
е . Papillae inside corolla along edges
1 E, 0.5 mm (at D); F, 0.25 mm (at D). Drawn from

d. —E

rona lobes. | ean find no reason not to reduce S.

calcarophilus to synonymy.
Tulear,

MADAGASCAR. N of

Spe € imen examined.
Ifaty, Bruyns 5954 (К).

al

—

1. Stapelianthus keraudreniae Bosser & Morat.
Adansonia, N. S., 11: 337, 339. 1971. TYPE:
Southwestern Madagascar. Betioky district,
Ankazoabo gorge, J. Bosser & P. Morat 19413
(holotype, Р not seen). Figure 11

Stems 25—150(-400) mm long, 4—10 mm thick,
forming dense to diffuse clumps, procumbent or
with erect apices, purple-brown flecked on gray-
green background, surface bullate: tubercles broad-
ly flattened-conical, weakly joined into 4 or 5(to 7)
angles along stem, tapering abruptly into small,
narrowly lanceolate, recurved leaf rudiment 1—2
mm long, which is somewhat flattened above and
gradually withers and falls off. Pedicel 3-7 mm
long, 1.5 mm thick, ascending to erect holding flow-
er facing upward; sepals 3—7 mm long, 1.5-2.0 mm
broad at base, ovate-lanceolate, acute, green suf-
fused faintly with purple. Corolla 20-35 mm diam.,
+ rotate; outside pale green finely spotted with red

to brown (often arranged in “veins”), with 3 to 5

Volume 91, Number 3
2004

Bruyns & Klak
Revision of Stapelianthus

raised longitudinal veins on each lobe, smooth: in-
side with scattered small obtusely conical usually
purple-tipped papillae becoming longest (up to 0.3
mm long) and densest along edges of lobes and in
mouth of tube but absent on outer side of annulus
(sometimes only along margins of lobes), each
tipped with small apical and often obtuse bristle,
annulus somewhat shiny, pale red to dark purple-
red or densely spotted with red-purple, lobes green-
ish to dull yellow spotted with wine- to purple-red:
tube + 3 mm long, 6-8 mm broad, pentagonal,
broadly V-shaped, containing gynostegium,
thickened into cushion-like raised circular annulus
around lobes 7-10 mm long, 8-12 mm

broad at base. ascending to spreading or recurved,

just
mouth:
ovate, acute, usually with reflexed tips: corona 3.0—

4.5 mm tall. red to dark maroon,

shiny, seated on very short stipe: outer lobes 3.0—

56 mm broad,
4.5 mm long, 2-3 mm broad, erect, spreading
above close to mouth of tube, slightly concave out-
side and convex within, bifid in upper quarter to
third into obtuse spreading to reflexed lobules: in-
ner lobes + 0.6 mm long, shorter than anthers, ob-
long-linear. Seed 5.0 X 2.5 mm, pear-shaped, swol-
len pale border, rest pale brown.

Distribution. Southwestern Madagascar. Eleva-
tion 50-320 m

Ecology. Stapelianthus keraudreniae is known
from areas apparently underlain by sandstones
(Rauh, 1998), where the plants grow in the shelter
of small bushes.

Discussion.
remarkably reminiscent of

audreniae are quite

those of, say, Huernia zebrina (except for being
much smaller) and are very pretty. As usual, there
is considerable variation in color, particularly from
dark to pale red, and the conspicuous, shiny an-
nulus may be spotted or uniformly red. The flowers
emit a faint bad odor of excrement, and some drops
of nectar-like secretion are sometimes found on the
annulus.

Specimens Pa big ADAGASCAR. SE of Tulear.

near Beza Mahafaly, P.R. yr s.n. me Beza Mahafaly.
18 Apr. 1987, Phillipson 1674 (TAN).

5. Stapelianthus insignis Desc., Naturaliste Mal-
gache 9: 181-182. 1957. TYPE: Southwestern
Madagascar. 21-23 km from
Tongobory near the Onilahy River, B. Desco-
ings 2751 (TAN missing) (lectotype. selected
here, Descoings (1957: fig. la—f)). Figure 12.

Tulear toward

ds ie ids insignis subsp. tongoboryenzis Rauh, Trop.
Subtrop. Pflanzenwelt 85: 36. 1993. Syn. nov. TYPE:

The flowers of Stapelianthus ker-

In deciduous forests near Tongobory, W. Rauh 21874
(holotype, HEID not seen).

Stems 50-200 mm long, 5-12 mm thick, pro-
cumbent to decumbent, often with apices ascend-
ing, (red-)gray- to cream-green marked with purple-
brown, surface bullate: tubercles broad and
flattened, somewhat joined into 4(or 5) rows along
stem so that stem is + square in cross section,
tapering abruptly into small, narrowly lanceolate.
spreading to recurved leaf rudiment 1-2 mm long.
which is slightly flattened above, gradually with-
ering and falling off. Pedicel 4-8 mm long, 1-2 mm
thick, ascending-erect and holding flower facing +
upward, sometimes longitudinally grooved, pur-
plish; sepals 5-8 mm long, 2-3 mm broad at base.

with
Corolla 17-26 mm diam.
panulate: outside pale green finely to boldly speck-

subulate narrow, slightly recurved apex.

smooth. at max.. bicam-

—

ed with purple; inside smooth except for few small
papillae along edge of corolla lobes, boldly speck-
led with purple on pale yellow-green: tube 5-10
mm long, 6—7 mm broad, cupular, fabric noticeably
thickened at mouth beyond which corolla widens
to maximum and then constricts to variable but
sometimes very narrow pentagonal mouth (6-16
mm diam.); lobes + 2-3 mm long, 3-10 mm broad
broadly and shortly triangular, acute, usu-
corona 4.5-6.0 mm tall, 4-6 mm
broad. dark maroon, seated on short stipe:
lobes 4.0-7.5

erect to slightly spreading, concave outside and

at base,
ally recurved;
outer
mm long, free practically to base.
with slight medial groove inside. deeply to only
shallowly bifid into + parallel lobules: inner lobes
+ 0.6 mm long. deltoid, obtuse, not usually ex-
ceeding anthers. Seed 5
shaped, very swollen border paler than rest.

X 3 mm, broadly pear-

Distribution. Southwestern Madagascar. Stape-
lianthus insignis is widely distributed, occurring
from the limestone hills just east of Tulear (and pos-
sibly further north as well) southward to Ejeda and
Ampanihy (Rauh, 1993: 36). Elevation 20-300 m.
Ecology. | Stapelianthus insignis occurs in flat
areas or on the lower slopes of hills. It always
seems to grow among pieces of limestone and small
bushes (very often a small, spiky member of the
Asteraceae) along the edges of denser bush.
Discussion. The flowers seem to be extremely
variable in color and also in the degree to which
they close up toward the mouth. Descoings's origi-
nal material was practically plain pale green out-
side with a very narrow mouth to the flower (+ 6
mm diam.). Some subsequent collections have had
a boldly spotted corolla (outside) with much broad-
er opening (up to 16 mm diam.). However, the type

432

Annals of the
Missouri Botanical Garden

Figure 12.
Side view of 1 ted flower.
Papillae biben еи 1 de a obe

|. Side view of ¢

removed. —

Stapelianthus dii "e Portion of stem. —B. ie 'e view of flower. —C. Side
Поу d gium.

» view of flower.

of gynostegium with one outer Pues lobe

—F Side vie
s. —H. Pollinarium. Seale bars: A, D, 3 mm (at A O

); 1
mm (at В); ^i 2 mm; F, 1 mm (at E); G, 0.5 mm (at P" н. 0.25 mm (at E). Drawn from A E. С. Н. PVB а rest,

hort. de Boer.

plant of Descoings came from the same area as the
newly described subspecies of Rauh (i.e... Tongo-
bory, near the Onilahy River) so that there is no
reason to believe that two geographically discrete
color forms are involved. In addition, flowers with
darkly and boldly mottled exteriors have also been
It would. be

found near La Table east of Tulear.

more reasonable to consider them all as variants of

a single species, and, consequently, Stapelianthus
insignis subsp. tongoboryensis is not recognized.
The buds of this species remain more or less
cylindrical until they are about 8 mm long, after
which the upper part begins to swell outward some-
what below the bases of the corolla lobes. This out-
ward swelling ultimately gives the corolla its bi-
'ampanulate shape and produces a bud with
roughly flat upper surface with the folds at the si-
nuses of the lobes projecting from this surface quite

close to its center and pointing in the direction of

the center, This is a most unusual arrangement: in

species with an annulus, such as Stapelianthus ker-
audreniae and various Huernias, these projecting
folds always remain beneath or at the edge of the
flat upper area in the bud. In other words, the ex-
pansion of the upper part of the corolla keeps up
with that of the lower: in S. insignis the lobes re-
main quite short so that the expansion of the lower
part of the corolla outpaces that of the lobes and
leaves them behind near the center of the bud.

The flowers appear to be odorless.

I have been unable to locate any material of the
type. This collection was illustrated in great detail
by Descoings, and so these illustrations are select-

ed as a lectotype.

Specimens examined. MADAGASCAR. Near Tulear,
coastal sea a Hardy & Rauh 2795 Var, 20 km E
of Tulear, Bruyns 6194 a (К); La Table, of Tulear,
Bruyns 5933 (ВО L); St po Bruyns P. (E). B
поку. Bruyns 5956 (PRE); Tongobory, Bruyns 5955 (MO)
E jeda, Bruyns 5957 (BOL)

Volume 91, Number 3 Bruyns & Klak 433
2004 Revision of Stapelianthus

| MI
| NW 1%, SU y

HO.
| *

Ke

Figure 13. Stapelianthus P dern —A. Side view of dissected flower. —B. Side view of gynostegium with one

outer corona lobe removed. —C. Papillae inside corolla near base of lobes. —D. Pollinarium. Se ale bars: A, 3 mm: В,
| mm: С. 0.5 mm (at B): p. 0.25 mm (at B). Drawn from hort. de Boer.

6. Stapelianthus montagnacii (Boiteau) Boiteau Morombe, 12 Apr. 1971, D. S. Hardy & Jacobsen
‹ > s s s. Ss
& Jean Bertrand. Cactus (Paris) 20: 6. 5559 lane. not seen: isotypes, FT not seen, К
not seen
1950. Stapelia montagnacii Boiteau. Bull. Tri-
mestriel Acad. Malgache, N.S. 24: 83. 1912. Stems 25-300 mm long, 6-10(-15) mm thick,

TYPE: Southwestern Madagascar. Near Tulear.
Dec. 1941 (f). P. Montagnac sub Jardin Bot.
Tananarive 4938 (TAN missing) (lectotype. se-
lected here, Cactus (Paris) 26: 116. photo by
G. Richard. 1950). Figures 13. 14, 15

procumbent often with ascending apices. mottled
with green to purplish on gray to cream back-
ground. surface bullate: tubercles broad and flat-
tened to conical, weakly joined into 4(to 6) angles

along stem. tapering abruptly into small. narrowly

Stape pice hard vi —€— Natl. Cact. Succ. J. 26: 67. lanceolate, recurved leaf rudiment 1-2 mm long.
J71. Syn. nov. TYPE: Western Madagascar. Near grooved above leaf rudiment, leaf rudiment slightly

Figure 14. >” s мине formerly known as S. hardyi.—A. Portion of stem. —B. Side view
of flower. —C. Side view of dissected flow an Side view of gynostegium With one outer Чаа m removed. —
E. P ); 1

apillae кА pcd near eei г lobe 5 . Pollinarium. Scale bars: A-C, 3 mm (at В); D. | mm; E, 0.5 mm
(at D); F. 0.25 mm (at D). Drawn n PVB 6200 |

434

Annals of the
Missouri Botanical Garden

Figure 15.
-F. 0.5 mm (at F);

but сой tube more mottle

flattened above and gradually withering and falling
off. Pedicel 7-12 mm long, 2.0-2.5 mm thick,
spreading and holding flower facing horizontally:

sepals 2.5-3.0 mm long, 1.5 mm broad at base,
ovate-triangular, acute, smooth, with recurved api-
ces. Corolla (13-)20-30 mm diam., shallowly cam-
panulate; outside maroon becoming cream with ma-
roon to red spots toward apex of lobes and base;
inside densely covered (in maroon portion except
at tips of lobes) with slender cylindrical maroon
papillae up to 3 mm long usually slightly thickened
toward apex and with spherical apical “bristle.”
maroon to red on lobes and onto mouth of tube,
below this cream concentrically speckled with ma-
roon to red becoming plain cream in base of tube;
tube 4-10 mm long, 9-17 mm broad, somewhat
thickened around mouth; lobes 6-9 mm long. 6-9
mm broad at base, deltoid, acute to acuminate,
erect to spreading; corona 4—6 mm tall, 6-8 mm
broad, dark red, seated on short stipe; outer lobes
4—5 mm long, free practically to base, erect, con-
cave outside and convex inside with groove down
middle, rather variably bifid in upper third into
erect deltoid lobules often with a smaller third one
between them; inner lobes + 0.5 mm long, + del-
toid, much shorter than to equaling anthers. Folli-
cles fusiform, with fairly stout horns diverging at +
150°, mottled with longitudinal
purple lines on a gray background; seed 5-7 X £

surface smooth.

Intermediates between ا‎ montagnacii and the former S. hardyi
—D-F. Papillae inside corolla along edges of lobes. —G.
2 0.25 mm (at F). 1

'd, outer corona lobes shorter, and papillae

= S. montagnacii]. —
Pollinarium. Sc ale
5 6203 eure to 5. hardyi
> with elongated apical bristle); B, C, E,

6195 (mixed population with smaller flowers more like typical S. montagnacii, papillae with variable apio sal 05

)rawn from A, D, б, PV

4.0 mm, pear-shaped, swollen pale-brown border,
rest darker brown.

Distribution. Southwestern Madagascar, from
southeast of Tulear to Morombe. Elevation 10-200 m.

Ecology. Stapelianthus montagnacii always
seems to occur in flat areas. Habitats vary from fine
sand in Didierea madagascariensis bush, to among
thick leaf litter on the floor of Euphorbia tirucalli
L.—E. intisy Drake thickets growing on loam. Plants
have also been seen in small pockets of soil on
limestone outcrops between stones and small bush-

~

as.

Discussion. There seems to have been some un-
certainty expressed in the literature about the dis-
tinctness of Stapelianthus madagascariensis and S.
montagnacii. Rauh (1963: 148) listed all the dif-
ferences that he could find between them. These
amounted to the slightly thicker stems (6-10 mm
thick) in 5. montagnacii (as opposed to 3-9 mm
thick in 5. madagascariensis), the slightly longer
corolla рае іп 5. montagnacii (the lobes measured
7-8 mm long and 7 mm broad in S. madagascar-
iensis, 6 mm long and 6 mm broad in S. montag-
nacii), the darker-colored corolla in S. montagnacii,
and the outer corona lobes that are only bifid in
the upper third in S. montagnacii (divided to the
middle in 5. madagascariensis). He concluded that
only one species was probably involved. Rauh

Volume 91, Number 3

Bruyns & Klak
Revision of Stapelianthus

Маре lianthus madagascariensis.—
'orona "r removed.

3 mm (at

Figure 16.
view of gynoste gium with one outer ¢
—E. Ры кайык. Seale bars: A, В,

5958

(1963: 148) mentioned also that S. montagnacii is
more difficult to cultivate than S. madagascariensis,
but this is a characteristic that is difficult to inter-
pret taxonomically, though it may be related to the
different edaphic conditions from which the plants
originated,

Rauh (1998) also suggested that Stape-
lianthus hardyi cannot be clearly separated from 5.

Later,

madagascariensis. However, the real problem with
S. hardyi is that it is not possible to separate it
from S. montagnacii. Stapelianthus hardyi shares
with S. montagnacii the slightly thicker stems, the
darker color of the corolla, and the outer corona
lobes that are only bifid in their upper third. The
main differences between them lie in the somewhat
darker, more deeply bowl-shaped flower of 5. har-
dyi, its slightly thicker corolla, the longer papillae
the
more massive outer corona lobes, and the

on the corolla with spherical apical “bristle.”
rather
larger pollinia. However, material gathered some 30
km north of Tulear (PVB 6195) is intermediate be-
tween the two in many respects. Here the flower is
not quite so dark and inside the mottling of maroon
on cream may continue right to the mouth of the
tube, the tube is shallower (at only 4-6 mm deep).
and the pollinia are smaller. For the present it
would seem that the most suitable arrangement is
to place S. hard yi and S. montagnacti together.
The type of this species is missing. А lectotype
is selected, using the illustration published by Boi-
teau and Bertrand (1950: 116).
explicitly stated as being of Montagnac 4938, it is

Although this is not

Face view of flower.
— 1).

A): C, | mm (at D):

—B. Side view of dissected flow

Papillae inside corolla around mouth " corolla tube.

D. 0.5 mm; E, 0.25 mm (at D). Drawn from PVB

assumed here that this photograph is of the material
on which Boiteau based his original description.
Specimens examined. MADAGASCAR, 2 km S of Mo-

rombe. Bruyns 6200 (MO); 40 km 5 of гуаг Bruyns
6203 (BOL); 30 km N of Tulear, Bruyns 6195 (BOL).

7. Stapelianthus madagascariensis (Choux)
Choux, in A. C. White & B. Sloane, Stape-
lieae, ed. 1: 71. 1933. Stapeliopsis madagas-
cariensis Choux, Compt. Rend. Hebd. Séances
Acad. Sci. Paris 193: 1444. 1931. TYPE:
Southern Madagascar. 15 km N of Ambovom-

1931, А. Decary s.n. (holotype, P not

seen). Figure 16.

be, Feb.

Stems 25-100 mm long, 3-9 mm thick, procum-

bent often with ascending apices, grayish marked
with purple-brown, surface bullate; tubercles broad
and flattened, very indistinctly joined into 4 to 6
tapering abruptly into. small,

1-2

mm long, which is slightly flattened above and

angles along stem,

narrowly lanceolate, recurved leaf rudiment
gradually withers and falls off. Pedicel 3-0 mm
long, 1.5 mm thick, spreading with erect apex hold-
ing flower facing upward; sepals 3-5 mm long, 1—
broad at base, ovate-lanceolate, acute,

Corolla 20-28 mm diam.,

panulate; outside pale green to cream spotted with

2 mm
smooth. shallowly cam-
maroon (spots becoming finer toward base and api-
ces of lobes); inside cream spotted with maroon
(fading away in tube), covered except in tube with
long, slender, white cylindrical papillae up to 2 mm

436

Annals of the
Missouri Botanical Garden

long with minute obtuse apical bristle; tube 4—7 mm
long, 10-12 mm broad, bowl-shaped: lobes 6-9 mm
long. 6-10 mm broad at base, broadly deltoid,
acute, spreading to recurved; corona 3.5—4.0 mm
tall, 4.5-6.0 mm broad, dark maroon, + sessile:
outer lobes + 3 mm long, free practically to base,
erect to slightly spreading. sometimes concave out-
side and slightly convex within, bifid at least to
middle, with lobules narrowly deltoid and slightly
diverging to obtuse and erect; inner lobes + 0.6 mm
long, narrowly deltoid to + linear, sometimes ex-
ceeding anthers. Seed 3.0-5.0 X 2.5 mm, shortly
pear-shaped, border slightly to very swollen, often
paler than rest.

Distribution. Southern Madagascar, coastal re-
gion from Ambovombe to Itampolo but also south-
east of Ihosy on southern edge of escarpment (Mor-
at, 1995). Elevation 50-800 m.

Ecology. | Stapelianthus madagascariensis may
grow among small bushes in denuded areas. How-
ever, plants seem to grow equally well in accumu-

lations of leaf litter on the floor of dry, xerophytic
forest.
Discussion. The stems of Stapelianthus mada-

rascariensis are generally prostrate with upturned
e P

4- to 6-angled. They

300 mm in di-

apices and are indistinctly
form dense mats that may reach
ameter.

Flowers of Stapelianthus madagascariensis are
shallowly bowl-shaped, cream inside, and spotted
all over with maroon. In some plants the spots fade
in intensity in the tube, while in others they coa-
lesce around the corona. Most of the inside (except
toward the corona in the tube) is adorned with long.
slender, often white, hair-like papillae. Outside, the
corolla is also spotted brightly with red, but these
spots do not correspond to those that are inside.

The outer corona lobes tend to be deeply bifid,
usually for at least half their length.

Stapelianthus madagascariensis is most closely
allied to S. montagnacii. The two species seem to
be reliably separable by the indistinctly angled, of-
ten quite slender stems and the shallowly bowl-
shaped flowers with small spots on a white back-
ground of S. madagascariensis. In S. montagnacii
the stems are usually thicker and fairly clearly 4-
angled, the flowers have a more deeply bowl-
shaped tube, and they are darkly colored with pale
mottling usually only near the base of the tube.

M examined. МАРАС, ipis
odona on road to Hampolo, 80 m. Labat, du Puy &
Phillipson 2096 (К); Tsihombe, Bruns 5958 (MO); 3-5
km from Behara, Sep. 1973, Rakotozafy 1238 (TAN); Am-
panihy, Bosser 19227 (Р)

pe tials,

0.5 km E of

HE rà ае.
— & $.

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teridae s.

, dn B. Bremer. 1997. Phylogeny of the As-

. based on rbcL sequences, with particular
reference to us Dipsacales. Pl. Syst. Evol. 207: 225-
25:

Bakker, ). Hellbrügge, A. Culham & M. Gibby.
1998. Pies netic relationships within sie
sect. Peristera (Geraniaceae) inferred oe nrDNA and
cpDNA sequence comparisons. Pl. Syst. Evol. 211:
273-287.

1992,

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Abbey
San Encino ЕЕ.

PHYLOGENY AND Katherine R. Gould? and Lena Struwe?
EVOLUTION OF

SYMBOLANTHUS AND

WURDACKANTHUS

(GENTIANACEAE-HELIEAE)

IN THE GUAYANA

HIGHLANDS AND ANDES,

BASED ON RIBOSOMAL

o8-NTS SEQUENCES!

ABSTRACT

—

Symbolanthus (Gentianaceae, Helieae) is a genus of small trees, shrubs, and herbs distributed in South America (the
central and northern Andes and the Guayana Highlands) and southern Central America. To discover the pattern of
Symbolanthus evolution and to assess the relationships m ‘tween Symbolanthus and the c а related Wurdackanthus
of the Guayana Highlands (Venezuela, Brazil) and the Lesser Antilles (St. Vincent), we performed cladistic analyses
on members of both taxa. Molecular data (5S- NTS rDNA sequences) were gathered from individual plant samples,
mainly from herbarium specimens. 55-NTS sequence data did not resolve internal relationships well in Symbolanthus
and show that the genus may be a recently and rapidly diverging clade. However, these results indicate that Wurdac
anthus is either paraphyletic to бааа or that W. argyreus is nested within a Symbolanthus clade. Fu 1
W. frigidus may be the basalmost species of the Wurdackanthus-Symbolanthus clade. This species is noticeab ly di-
vergent and. distinct, molecularly and ud. from the rest of б clade. Testing an alternate phylogenetic
hypothesis in which Wurdac irte is monophyletic results in trees 11 steps longer than the shortest trees found, and
still with Wurdackanthus nested within Symbolanthus. ~ estral bes ‘al character evolution in the Wurdackan-
оо 5 is disc iei in the context of a 5S-NTS consensus tree.

ey

we 98-NTS, biogeography, Gentianaceae, Helie 'ae, molecular systematics, morphology, Neotropics, phylog-
eny, ет ВА Wurdackanthus.

RESUMEN

El género Symbolanthus (Ge ш eae, Helieae) incluye árboles pequeños, arbustos y hierbas, distribuidos en Sur
América (al centro y norte de es y en las tierras altas de la Guayana) y al sur de Centro América. Con el objeto
de descubrir el patron de la evo ine ібп y biogeografía de Symbolanthus, realizamos un análisis cladístico pe algunas
especies de Symbolanthus y del cercanamente relacionado W pi сен distribuido en las tierras altas de la Guayana
(Venezuela, Brazil) y en las Antillas Menores (St. Vincent). Los datos moleculares (secuencias de 58-N' IS 1 on se
obtuvieron de muestras individuales de plantas, principalmente de especimenes de herbario. Las secuencias de 5S-
NTS no resolvieron bien las relaciones al interior de Symbolanthus, y mostraron que el género puede haber divergido
рев. y recientemente. Estos resultados indican ya sea que Wurdackanthus es parafilético respecto a Symbolanthus, o
que argyreus se encuentra dentro del clado de Symbolanthus. Mas aún, W. frigidus podria ser la especie más basal
del alado Wurdackanthus-Symbolanthus. Esta especie es notoriamente diferente, tanto molecular como morfológica-
mente del resto del clado. A probar una hipótesis alterna, en la cuál Wurdackanthus es monofilético, se encuentra
árboles 11 pasos más larges 4 que los mas cortos obtenidos, atin con Wurdackanthus incluído dentro de E
Con base en el consenso obtenido usando 5S-NTS, se discute la evolución de caracteres morfológicos ancestrales en
el c lado Wurdackanthus—Symbolanthus.

=

' We thank the Pda of AAU, BM, К, HUH, К, MO, NY, 5, U, US, USM, and WU for iig of plan material to
LS, and NY and US for permission to remove leaf material from their sheets for DNA extraction. We are also grateful
to Paul Berry for insi comments on the manuscript, Jason R. Grant for unpublished information, E Rocio Cortez
for Spanish translations. This work was funded by the National Science Foundation (award 0317612 to LS), Rutgers
University, New Brunswick, New Jersey, and the Lewis B. and Dorothy Cullman Program for Molecular Systematics
Studies, The New York Botanic 2 Carden New York.

? Department of Biology, Wes Carolina University, 132 Natural Science Building, Cullowhee, North Carolina
28129, U.S.A. kmathews@e maily wcu.edu.

Author for correspondence: Depa riment of Ecology, Evolution and Natural 5 Rutgers University Cook
C ш ge, 237 Foran Hall, 59 Dudley Road, New Brunswick. New Jerse y 08901, U.S.A. struwe@aesop.rutgers.edu.

ANN. MISSOURI Вот. GARD. 91: 438-446. 2004.

Volume 91, Number 3
2004

Gould & Struwe
Phylogeny of Symbolanthus

439

Symbolanthus G. Don (Gentianaceae) is a genus
of about 30 species of small trees, shrubs, and
(rarely) herbs distributed mainly in montane rain
forests in the northern and central Andes (Bolivia,
Colombia, Ecuador, Peru, Venezuela: ca. 21 spp.)
and the Guayana Shield highlands in South Amer-
ica (Brazil. Guyana, Venezuela; 7 spp.). as well as
southern Central America (Costa Rica, Panama; ca.
2-3 spp.). The Guayana Highland is one of the old-
est land regions in South America, part of the orig-
inal Gondwanan continent, which has not been in-
undated since the mid-Cretaceous (100 mya:
Huber. 1995). The highland region comprises table
mountains, known as tepuis, up to 3014 m altitude.
Most tepuis consist of sandstones of the Roraima
Formation overlying the Precambrian crystalline
1985).
The age of the uplift of the sandstone plateau is

—

basement of the Guayana Shield (Ghosh,

unknown, but cycles of upheaval and erosion may
go back to the Mesozoic (Kubitzki, 1989). Erosion
of the sandstone resulted in the formation of iso-
lated, vertical-cliffed mountains, the tepuis
Symbolanthus is a member of the well-defined
Helieae clade, which primarily consists of Adeno-
lisianthus (Spruce ex Prog.) Gilg, Aripuana Struwe,
Maas & V. A. Albert,
nanthus eek zilg, Helia Mart., Irlbachia Mart.
Macrocarpaea (Griseb.) Gilg, Rogersonanthus Ma-
guire & B. M. Boom, Symbolanthus, Тасма Aubl.,
. M. Ep and Wurdac-
2002). He-

lieae are exclusively Neotropical et the. highest

Calolisianthus Gilg, Chelo-

Tetrapollinia Maguire &
kanthus Maguire (Struwe et al., 1
concentration of genera on the Guayana Shield.
They include the majority of non-montane Neotrop-
ical gentians and contain among the highest mor-
phological and anatomical diversity within the fam-
ily. Many Helieae, as well as Symbolanthus, species
are endemic to single mountain tops, ridges or mas-
Sils. river drainages, or islands. Symbolanthus in-
frageneric taxonomy is fraught with difficult species
delimitation problems, particularly among Andean
entities. and many undescribed species (Struwe,
2003a, b).

Symbolanthus and the morphologically similar
Wurdackanthus together form a well-supported
2002: Fig. 1).

can be distinguished from other Helieae and

—

clade within Helieae (Struwe et al.,
They
gentians by pollen morphology and the presence of
a corona or corona-like structure within the corolla.
Wurdackanthus differs from Symbolanthus in hav-
ing a much shorter calyx that is divided % of its
length, as opposed to being divided 7, or more of
its length (Pringle, 1995: Struwe et al., 1999). Wur-

dackanthus consists of two species, W. argyreus,

which is endemic to the Guayana Highlands, and
W. frigidus, found in the Lesser Antilles.

Our objectives in this study are to determine the
phylogenetic relationship between Symbolanthus
and Wurdackanthus, which share morphological
characteristics that are unique within Helieae, and
to investigate these putative synapomorphies in a
phylogenetic context with a known outgroup, Che-
2002).

analyses of Helieae with nrDNA sequences of the

lonanthus (Struwe et al., Previous cladistic
internal transcribed spacer (ITS) region showed
that this gene region, though highly variable in oth-
er Helieae lineages, including Macrocarpaea (Grant
& Struwe, 2000),
Symbolanthus to resolve interspecific relationships
(Struwe et al., 2002; Fig. 1). In order to assess re-
lationships within Symbolanthus, it was necessary

does not vary enough within

to use a more quickly evolving DNA fragment.
DNA of the ribosomal 58 non-transcribed spacer

5S-NTS) region has been shown to be highly var-

pm

iable in closely related species of plants (e.g.. Ali-
bertia A. Rich., Persson, 2000; Saintpaulia Wendl..
Lindqvist & Albert, 1999; see also Cox et al., 1992;
Kellogg € Appels, 1995; Cronn et al.. 1996). Like

ITS sequences, SS-NTS sequences are arranged in

arrays of several hundred to several thousand tan-
demly repeated copies that occur at one or several
chromosome loci and that normally become homog-
enized via concerted evolution processes (Hillis &
Dixon. 1991; Playford et al., 199:

MATERIALS AND METHODS
MOLECULAR METHODS

Due to the remote habitats of many Symbolan-
thus and Wurdackanthus species, we relied on DNA
extraction from leaf material from herbarium sheets
(Table 1)
dried leaf tissue. Leaves were pulverized by means
of a Bio 101/Savant FastPrep tissue disruptor, fol-
lowed by extraction with a CTAB (cetyldimethylam-

Total DNA was extracted from 0.5-1 em?

monium bromide) buffer with the addition of 1%
PEG 4000 (polyethylene glycol), and glassmilk
(GeneClean, Bio 101) purification (modified from
Struwe et al., 1998). For difficult samples, a chlo-
roform:isoamyl alcohol (24:1) purification step was
added following CTAB extraction. Amplification of
the 5S-NTS
(PCR) was accomplished in standard 25 pl reac-
tions on a Perkin Elmer Gene Amp 9600 in the

region by polymerase chain reaction

presence of bovine serum albumin (BSA, 0.04%)
and tetramethyl ammonium chloride (TMACI, 0.1
mM). Бен primers were “55 forward" and 755 re-
verse" designed by Cox et al. (1992). The cycle
program included an initial incubation at 95°C for

Annals of the

440
Missouri Botanical Garden

Macrocarpaea

clade
L-

Irlbachia clade Irlbachia (3 spp.)
[^ Aripuana cullmaniorum

LL Chelonanthus purpurascens

| iChelonanthus alatus.
Tetrapollinia caerulescens
Calolisianthus (2 spp.)
Chelonanthus angustifolius
iChelonanthus albus:

1 Chelonanthus viridiflorus

Chorisepalum (1 sp.)

Tachia (3 spp.)

Macrocarpaea (6 spp.)

Symbolanthus
clade

Symbolanthus sp.
Symbolanthus pulcherrimus

Wurdackanthus frigidus

> 1. Pre AE phylogenetic re 5 of the Helieae based on ITS sequences (adapted after Struwe et
al. poss and L. V Grant & У. A. Albert, unpublished). Within Helieae, three major well-
«s 'd clades are Pide milie d. the М: acrocarpaea clade, the Irlbachia clade, and the Symbolanthus clade (Struve et
2002). The genus Chelonanthus is paraphyletic within the Symbolanthus clade; the two species used in this study

are » indie id with dotted boxes. The Symbolanthus-Wurdackanthus clade is indicated with a solid box

~

vould,

the same PCR primers. Sequencing reactions were
cleaned by means of Sephadex (Pharmacia Biotech
AB) column purification.

Sequencing gels were run on an ABI 377 XL au-

2 min., followed by 27 cycles of 94°C for l min.,
60°C for 1 min., and 72°C for 1 min.

Most PCR products were run on a low-melting
agarose (1.2%) gel, from which the fragments were
plugged, resuspended in 300 ul water, and ream-
plified as before to increase product yield. PCR
products were then prepared for sequencing by col-

tomated sequencer. Sequences obtained were edited
and aligned using the software program Sequencher
3.0 (GeneCodes Corp.). Only clearly readable se-

umn purification using QlAquick spin columns
(Qiagen). This was followed by PCR-based cycle
sequencing reactions using a d-Rhodamine Termi-
nator Cycle Sequencing Ready Reaction kit (Perkin
Elmer Applied Biosystems) with AmpliTaq DNA

polymerase, FS, following kit protocols, and using

quences were used. The aligned sequences were cut
at an arbitrarily chosen position at both ends of the
spacer where all sequences were readable. The com-
plete alignment at <http://www.rci.
rulgers.edu/~struwe/dnadata.htm>. All molecular-
based phylogenetic work was done at the Lewis B.

is available

Volume 91, Number 3
2004

Gould & Struwe
Phylogeny of Symbolanthus

and Dorothy Cullman Program for Molecular Sys-
tematics Studies of the New York Botanical Garden.
Table 1 lists the species, voucher specimens, and
Genbank accession numbers of sequences used 1
the study.

Eleven individuals and nine species of Symbo-
lanthus and both species of Wurdackanthus were
sampled. Attempts to amplify 55-NTS for additional
species of Symbolanthus from herbarium material
(in particular from tepui species) failed, presum-
ably due to poor specimen preservation, Two spe-
cies of Chelonanthus were used as outgroups fol-
lowing sister-group relationships derived from ITS
data (Struwe et al., 2002; Fig. 1). Thus a total of
15 individuals representing. 13 species were in-
cluded in the 58-NTS data set. Species of Caloli-
sianthus and Tetrapollina caerulescens (Aubl.) Ma-
guire & В. M.
5S-NTS. but were very divergent from and therefore
difficult to align. with Symbolanthus and Chelo-
nanthus and were not included in the analysis. Dur-

Boom were also sequenced for

ing the course of this study. four undescribed spe-
cies of Symbolanthus were identified among our
herbarium samples. They are here indicated as “sp.
ined. 1-4” (Table 1) and will be described in a later
publication on the taxonomy of Symbolanthus.
Phylogenetic analyses were done using maximum
UP* version 4.0b4a (Swofford,
2000). Minimal length trees were searched for us-
ing the heuristic option, with TBR branch-swap-
ping, 100 replicates of random addition sequence

parsimony in

order, and branches bid if the maximum
branch length is zero. Gaps in the aligned 55-NTS
sequences were treated as missing data. Branch
lengths were calculated using the ACCTRAN op-
tion in PAUP*

Internal clade support was evaluated using the
parsimony jackknifing procedure, which was per-
formed in Хас (Farris et al.. 1996), using 1000 rep-
licates with 5 random addition replicates each. De-
cay analyses (Donoghue et al., 1992) were done in
PAUP* by means of the AutoDecay program (Eriks-
son, 1998). In addition, analyses were run with to-

pological constraints imposed, first forcing Wurdac-

—
~
х

kanthus and then Symbolanthus to

monophyletic, to determine their effects on tree
lengths and to test alternate hypotheses of relation-
ships. Heuristic searches were done with these con-
straints imposed and all other run options as above.

MORPHOLOGICAL METHODS

Morphological data were collected by examining
the same specimens that were sequenced, as well
as duplicates of the same collections and pickled

flower and fruit material from the same collection
when available. Output trees from PAUP* were im-
ported into MacClade version 3.084 (Maddison «
Maddison, 2000) in order to explore changes among
morphological character states. Thirty vegetative
and reproductive characters were examined, in-
cluding five quantitative characters. Measurements
for quantitative characters were divided into dis-
crete ranges by means of two different methods de-
Chappill (1989) (gap-coding and seg-

ment-coding) and coded as discrete character

scribed
stales.
RESULTS
DS-NTS
The aligned data set of the 55- МГУ region con-
ains 322 characters, including 139 (43%) variable

characters and 55 (17%) parsimony-informative
characters.

However, most of the variation found
represents differences between the outgroup, Che-
lonanthus. and Wurdackanthus—Symbolanthus, as
well as between W. frigidus and the remaining in-
group taxa (see below). Individual sequence lengths
for the 58-NTS region range from 292 bp (Chelo-

nanthus alatus) to 311 bp (Symbolanthus nerioides

—
"

with most taxa having a length of 308 bp. Mean
GC content for the data set calculated in PAUP* ts
57%.

PARSIMONY ANALYSES

Results of the parsimony analyses are shown in
Figure 2. The parsimony analysis of the 55-NTS
data set alone yielded 42 shortest trees of length
186 (consistency index excluding uninformative
characters (CI) = 0.86, retention index (RI)
0.85; Fig. 2A. B). In the strict consensus tree (Fig.
2A), with Chelonanthus spp. as outgroup. Wurdac-
kanthus frigidus (St. to the re-
maining taxa, with 100% jackknife support and a
decay value of 30. Wurdackanthus argyreus (Gua-
yana Highlands: Sierra de la Neblina and Cerro
Aracamuni) and all Symbolanthus species form a
clade (jackknife = 100%, decay = 8) within which
there is little resolution. However, two clades with

Vincent) is sister

good measures of support are found, one containing
the two 5. macranthus samples (Ecuadorean cloud
jackknife = 73%),
containing two Central American species, S. pul-
cherrimus (Cartago region of Costa Rica) and S. sp.

forest species: and a second

ined. 1 (Veraguas, Panama) (jackknife = 98%, de-
cay — 4). Overall, there is relatively little molecular

divergence within the W. argyreus + Symbolanthus
clade, with the exception of a long terminal branch

Missouri Botanical Garden

Annals of the

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Volume 91, Number 3
2004

Gould & Struwe 443
Phylogeny of Symbolanthus

A
d30, 100

— 5 changes

Figure 2.

— € Chelonanthus alatus
Chelonanthus albus

d4, 98

Results of analyses of Symbolanthus-Wurdackanthus based on 55-NTS sequence data. —A.

Wurdackanthus frigidus

r— — Wurdackanthus argyreus
Symbolanthus vasculosus
Symbolanthus sp. ined. 2
Symbolanthus sp. ined. 3
Symbolanthus sp. ined. 4

— Symbolanthus nerioides 1
d8, 100

Symbolanthus nerioides 2
Symbolanthus brittonianus
AC Symbolanthus macranthus 1
Symbolanthus macranthus 2
— Symbolanthus pulcherrimus
Symbolanthus sp. ined. 1

C. alatus

C. albus
W. frigidus
S. macranthus 1

S. macranthus 2
S. sp. ined. 2
W. argyreus

S. vasculosus

S. nerioides 1

S. nerioides 2

S. brittonianus

S. sp. ined. 3

S. sp. ined. 4
S. pulcherrimus

S. sp. ined. 1

Strict con-

sensus tree showing support indices for no xles i including decay values greater than 1 (preceded by “d”) and jackknife

values greater than or equaling 5096. —B.

analysis

leading to Symbolanthus sp. ined. 4

(Bolivian An-

тее showing branch lengths for one of 42 shortest trees from the 5S-NTS

CONSTRAINT ANALYSES

Notably,

there is a relatively large amount of divergence be-

des), containing 28 changes (Fig. 2B).

tween the two species of Wurdackanthus, with a
long branch containing 13 changes between W. fri-
gidus and W. argyreus + Symbolanthus.

The first constraint analysis kept only trees com-
patible with a pre-defined Wurdackanthus mono-
phyly constraint tree. PAUP* found 491 trees of
length 197, 11 steps longer than the most parsi-
monious trees (CI = 0.76, RI = 0.71). In all of

444

Annals of the
Missouri Botanical Garden

these trees, a Wurdackanthus clade is nested within
a Symbolanthus clade, making Symbolanthus pa-
raphyletic.

The second constraint analysis kept only trees
compatible with a pre-defined нок mono-
phyly constraint tree. PAUP* found 30 trees of
length 187, one step longer than the most gaii
0.85, RI 0.84).
these trees, Wurdackanthus is paraphyletic toward

monious trees (CI

Symbolanthus, with W. frigidus most basal followed
by W. argyreus.

In summary, results indicate that Wurdackanthus
is paraphyletic, with W. frigidus sister to a M. argy-
reus + Symbolanthus clade. Wurdackanthus argy-
reus is either sister to the Symbolanthus species or
nested among them. The constraint analysis forcing
Wurdackanthus
much longer than the most parsimonious trees and

finds trees

-

o be monophyletic
results in a non-monophyletic Symbolanthus.

MORPHOLOGICAL ANALYSES

Eight characters out of 30 that were examined
were found to be potential synapomorphies for
clades. These characters were corolla length, calyx
length, depth of calyx division, number of flowers
per inflorescence, capsule length, pollen type, pres-
ence of corona or staminal pockets inside the co-
rolla, and flower bud shape (see Fig. 3). The dif-
ferent means of coding quantitative character states
did not affect the outcome of the analysis of syna-
pomorphies.

DISCUSSION
PHYLOGENY

Sequencing of the 5S-NTS region has now been
done within three genera of Helieae, including the
two largest, Symbolanthus and Macrocarpaea. We
expected 5S-NTS data to be useful for resolving
both higher- and lower-level relationships. For ex-
ample, the 5S-NTS data do indicate the paraphyly
of Wurdackanthus toward Symbolanthus. Because a
monophyletic Wurdackanthus is not supported by
these data, and because of its morphological and
anatomical similarities to Symbolanthus, its cireum-
scription should be reconsidered (Struwe & Gould,
2004

However, we found that in Helieae, 5S-NTS data
also highlighted the accumulation of different
amounts of molecular change lineages of pre-
sumably different ages. While there is little varia-
tion within Symbolanthus, considerably more vari-
ation occurs within Macrocarpaea (J. R. Grant & L.
which based on relative

Struwe, unpublished),

In all of

amounts of ITS variation (Grant & Struwe, 2000) is
estimated to be a relatively much older lineage.
We did find a relatively large amount of molec-
ular change between Chelonanthus and Wurdac-
kanthus—Symbolanthus (branch length = 39),
well as between the two species of Chelonanihus
27: see Fig. 2B), in-
dicating that the 5S-NTS region can be useful in

we sampled (branch length =

phylogenetic studies at higher levels, e.g., between
closely related genera. Many changes also occurred
along the branch between Wurdackanthus frigidus
and W. argyreus + Symbolanthus (13), signifying a
greater divergence between the two species of Wur-
dackanthus than between W. argyreus and Symbo-
lanthus spp.

MORPHOLOGY

Compared to the outgroup, Chelonanthus, poten-
Wurdackanthus—
Symbolanthus clade include having long corollas

tial synapomorphies for the
(greater than ca. 3 cm) and relatively large cap-
sules. Other synapomorphies that distinguish Wur-
dackanthus—Symbolanthus from all other Helieae
are common presence of a corona or staminal pock-
ets inside the corolla and pollen of Symbolanthus-
type (i.e., pollen grains united in tetrahedral tetrads
with strongly reticulate exine; Nilsson, 1970) (Fig.
Potential synapomorphies for the Wurdackanthus
argyreus + Symbolanthus clade include even lon-
ger corollas (5.7 cm long or greater), pointed flower
bud apices, and 1 to 3 flowers per inflorescence

(vs. 5 or more) (Fig. 3). Chelonanthus bears many
flowers per inflorescence on 1 to 4 long monocha-
and Wurdac-

kanthus frigidus produces up to 7 flowers on mono-

sial branches within a dichasium.

chasial branches, while Wurdackanthus—
Symbolanthus have reduced 1- to 3-flowered mono-
or dichasia. Deeply divided calyces is another pos-
sible synapomorphy for the W. argyreus + Symbo-
lanthus clade (calyces divided 2/3 to nearly all the
way to the base vs. 1/3 divided in W. frigidus; Fig.
3). but Chelonanthus is polymorphic for this char-
acter.

These morphological changes, as well as the rel-
atively large number of nucleotide base changes
along the branch to this clade, indicate that Wur-
dackanthus argyreus and W. frigidus are relatively
divergent from one another. The character of calyx
length has been used in the literature to separate
Wurdackanthus from Symbolanthus, Symbolanthus
having a longer calyx (e.g.. Pringle, 1995; Struwe
et al.,
relatively short calyx of Wurdackanthus is a plesio-

1999). However, according to our results, the

Volume 91, Number 3
2004

Gould & Struwe 445

Phylogeny of Symbolanthus

sg Chelonanthus alatus

К Chelonanthus albus

Wurdackanthus frigidus

Wurdackanthus argyreus

Symbolanthus vasculosus

—
ZZ

Symbolanthus sp. ined. 2

* Corollas >3 cm

Symbolanthus sp. ined. 3

* Large capsules

Symbolanthus sp. ined. 4

Symbolanthus nerioides 1

* Corona or staminal pockets

Symbolanthus nerioides 2

e Symbolanthus pollen type

Symbolanthus brittonianus

* Long corollas (75.7 cm)

* Pointed flower buds

* Few-flowered inflorescences
* Deeply-divided calyces?

Symbolanthus macranthus 1
Symbolanthus macranthus 2
Symbolanthus pulcherrimus

Symbolanthus sp. ined. 1

Long calyces

Figure 3. Potential morphological аш for Wurdackanthus + Symbolanthus, W. argyreus + Symbolan-

thus and Symbolanthus based on the 5S-NTS

morphic character state that is also found in Che-
lonanthus. not a synapomorphy for Wurdackanthus
(Fig. 3). Although the two species of Wurdackanthus
are relatively divergent from one another morpho-
logically and in 5S-NTS sequences, other molecular
data sets support a close relationship between W.
frigidus and Symbolanthus spp. (nr TS sequences
and cpDNA tral et al.
2002).

intron sequences, Struwe

BIOGEOGRAPHY

The Symbolanthus distribution is an excellent
opportunity to test the influence of migration be-
Andes,

Central America, and to test biogeographic hypoth-

tween the Guayana Highlands, the and

eses about the origin of the Guayana Highland flo-

This study indicates the possibility that tepui
species could have had Andean origins, since Wur-
dackanthus argyreus (Sierra de la Neblina and Cer-
ro Aracamuni) is not consistently basal but nested
Symbolanthus species. In the

among non-ltepul

50% majority rule consensus tree. il is nested

triet Consensus t

among two Venezuelan Andean species (S. nerioides
and 5.
this group would be to obtain better material of

vasculosus). Future research directions on
tepui species for DNA sampling, or use morpholog-
ical data to make a phylogeny of all species once
a revision of Symbolanthus is complete (Struwe, in
prep.). In addition.

such as KLs.

a higher-resolution data set.
would probably be helpful.

Literature Cited

Chappill, J. A.
netic c* pd Cladistics 5: 2 —2:

Cox, A . D. Bennett & T. A. Dyer. 1992. Use of the
ote tn rase chain reaction to Wet | spacer size hetero-

gene clusters and to loc ate

1989. Quantitative characters in phyloge-
234.

=

geneity in plant 5S-rRNA

such clusters in wheat (ticum aestivum L.). Theor.
Appl. Ge н. s 83: 684—6
Cronn, R. C. Zhao, A. a en. & J. E Wendel.

1996. Polymorphism a concerted evolution in a tan-

demly repeated gene family: 5S ribosomal DNA in ОЕ
loid and RE cottons. J. Molec. Evol. 42: 685
705.

Donoghue, . Olmstead, J. mith & J.
Palmer. el a dE netic re p Sa of Dipsac Bes "s

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based on rbcL sequences. Ann. Missouri Bot. Gard. 79:
333-345.

Eriksson, T. 1998. AutoDecay vers. 4.0. Department of
Botany, Stockholm University, Stockholm. [Distributed
by the author,

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in

А Albert, M. Küllersjó, D. Lipscomb &
S King; 1996. Parinom atras outperforms

ne boring Cladistics 12: 99—

Ghosh, S. K. 198 robo of the ена group and its
implic ations. Pp. 33-50 in M. I. Muñoz (editor), I Sym-
posium Amazónico. Minit ria de Energía y Minas, Re-

pública de Venezuela, Caracas.

Grant, J. R. & L. Struwe. 2000. Morphological evolution
and Ne 'otropic w bioge qud in Macroc о oer
naceae: Helieae . Bot. 87 (suppl.): 1

.&

Hillis, D. үө 1991. Ribosomal in A: M
lecular e ation and num netic inference. Quart.
Rev. Biol. 66: 411—415:

Huber, О. Tes Ge vili ‘al and physical features. Pp.
1-61 in Р. E. Berry, В. K. Holst & K. Yatskievych (ed-
itors), Flora of the Vene n Guayana, Vol. 1. Mis
souri Botanical Garden Press, St.
Press, Portland.

Kellogg, E. A. & R. Appels. 1995. Intraspecific variation
in 5S RNA genes are decoupled in diploid wheat rel-

)
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atives. E netics 140: 325-343,

Kubitzki, K. 1989. The ecogeographical diffe Epa of
кс, inundation forests. Pl. Syst. Evol. 162: 285—
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Lindqvist, C. & V. A. Albert. 1999, Phylogeny and con-
servation of African violets (Saintpaulia: Gesneriaceae):
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cribed spacer e: nces, Kew Bull. 54: 363-377.

Maddison, V P & D. R. Maddison. due as lade vers.
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Massachus

pie n LS al „а to
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n 64: 1—

). Phyloge ny P the Neotropical Alibertia

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Playford, i R. В & В. k. йаш. 1992. The 58 units

of Acacia species (Mimosaceae). РІ. Evol. 183:

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I 59A. Department of Systematic Botany, Góteborg Uni-
versity, Góteborg.

Struwe, L. 2003a. Revision of Bolivian N
AA Harvard Pap. Bot. 8(1):

. 2003b. Two new winged species of Symbolanthus
(Gentianaceae: Helieae) from Colombia. Novon 13
133-1. 10.

— . R. Gould. 2004. Redefinition of Symbolan-
thus io inc dude Wurdackanthus (Gentianaceae—Helieae).
Novon 14: 354—359

P. J. M. Maas & V. A. Albert. 1997, Aripuana
cullmaniorum, a new genus and species of Gentiana-
ceae from white sands z southeastern Amazonas, Bra-

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—, M. Thiv Kadereit A. S-R. Pepper, T. J. Motley,
Р J. White Н. E. Rova, K. Potgieter & V. A. Albert

1998. Saceifolium | ieri ceae), an endemic of Si-
erra de la Neblina on the Brazilian Venezuelan frontier,
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ceae. d Be E 3: 199-2] т
‚ P. J. M. Мааз, О. Pihlar & У. A. rt. 1999,
Gentiana eae. gom 47. 542 1 у» ITY ‚ Holst

& K. Yatskievych (editors), Mon
a Vol.
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character evolution, and biogeography of Gentianaceae,
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Swofford, D. L. 2000. PAUP* (Phylogenetic Analysis Us-
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nauer, Sunderland, Massachusetts.

VIII INTERNATIONAL AROID
CONFERENCE, MISSOURI
BOTANICAL GARDEN, ST.
LOUIS, 9-11 AUGUST 1999:
INTRODUCTION

Thomas B. Croat!

The УШ International Aroid Conference. orga-
nized by Tom Croat of the Missouri Botanical Gar-
den, was held in August 1999, the week following
the XVI International Botanical Conference in St.
Louis. Over 125 attendees from 21 countries par-
ticipated in three days of paper sessions, poster
presentations, greenhouse tours, and social events.

Oral presentations were made in six general ar-
eas: 1. Araceae of general areas, including aroids
in South America, the Mediterranean Region, North
America, the Indian Africa.
Madagascar. 2. Aroid collections, horticultural and
herbarium, including South Florida, Marie Selby
Botanical Gardens, the Royal Botanical Garden,
Kew, the botanical gardens in Munich and Brus-
sels, Russia, and Australia. A special presentation
was made by Tony Avent of Juniper Level Botanical
Garden. 3. Morphology, systematics, and evolution,
including papers on Rhodospatha, Raphidophora,
Philodendron subg. Pteromischum, Amorphophal-

Subcontinent, and

lus, Arisaema, Dracontium, shoot morphology in
Brazilian root-climbing Araceae, comparative veg-
elative anatomy, and molecular systematics of the
Caladium alliance. 4. Araceae of specific areas, in-
cluding papers on the Araceae of the Flora of Chi-
na, Brunei, central Brazil, Ecuador, Thailand,
Western Ghats, India, Bajo Calima in Colombia, Vi-
etnam, and Chiapas State in Mexico. 5. Aroid
breeding and horticulture, including research with
potted ornamental plant breeding, the Anthurium

cut-flower industry in Holland, taro production in

Hawaii, micropropagation of Araceae, biotech
breeding of Anthurium, and cultivation of Arisaema.
Miscellaneous, including papers on pollination
ecology of the Araceae, insects associated with Ar-
aceae, registration of hybrid plants, investigations
1 Arum, studies with tribe Lasioideae, Amorpho-
phallus in China, acids of seed lipids in Araceae,
comparison of two models for chromosomal evolu-
tion in Araceae, revision of Homalomena, taxonomy
and phylogeny of Philodendron sect. Calostigma in
Brazil, Aroid-L and the International TAS Society
webpage, and finally, a roundtable discussion of the
IAS webpage development.

A total of 45 posters were presented on a wide
variety of subjects dealing with Araceae and were
displayed during all three days of the conference.

The scientific papers presented in this issue were
among the presentations at the conference; the re-
maining papers will be published in Aroideana.
The offerings included here are Felipe Cardona's
“Synopsis of the genus Spathiphyllum (Araceae) in
Colombia”; Eduardo С. Gongalves’s “Araceae from
Brazil: Comments on their diversity and
biogeography”: J. Henny et al.’s “Progress in
ornamental plant breeding research”; and three pa-
Araceae,

central

yers addressing anatomical research of
namely, Eduardo G. Goncalves et al.’s “A prelimi-
nary survey of petiolar collenchyma in the Ara-
ceae," and Richard €. Keating “Vegetative ana-
tomical data and its relationship to a
classification of the genera of Araceae” and “Sys-
tematic occurrence of raphide crystals in Araceae.”

revised

Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A. thomas.croat@mobot.org

Ann. Missourt Bor. GARD. 91: 447. 2004.

SYNOPSIS OF THE GENUS Felipe Cardona?
SPATHIPHYLLUM (ARACEAE)
IN COLOMBIA!

ABSTRACT

The last revision of ii. ич was published over 40 years ago, and there is considerable need for additional

new work throughout the tropics. Preliminary results are here presented toward the genus یی‎ ai in Colombia,
where 18 of the 50 known species occur. In fis ui. 'al region, all species appear restricted to the lowland to
middle-elevation forests of interandean valleys, Amazonia and Chocó regions, from sea le Meg to 1300 m. The middle
tío Magdalena valley in ا‎ rn C кж with 9 species, exhibits the highe st concentration of taxa. Species of
eru rh grow in partially r periodic ‘ally flooded primary forests and in sites with low light intensities. Four
sections of the genus Sapo lam о, occur in Colombia: sect. e үт sect. Massowia, sect. M
and sect. Spatium Five species are from elsewhere in the Amazonian region of South America, and 11 othe
species appear widely dia tributed i intral America.

Key words: Araceae, Colombia, Смет ша

RESUMEN

La última revisión de Каш eo fue pube ada hace 40 años у hay una considerable necesidad de nuevos trabajos
para el trópico. Se presentan los resultados preliminares. para el género Spathiphyllum en C — donde el género
está represe miado por 18 de las 50. especies conocidas. En esta región geográfica todas las especies están жа ы
а los bosques de tierras bajas de los valles interandinos, la Amazonia y la región del Chocó, dade el nivel del mar
hasta 1300 m. El valle medio del Río Magdalena en el NO i país, con 9 especies, presenta la más alta concentración.
as especies de Spathiphyllum crecen en sitios parcial o periódicamente inundados con bajas intensidades de luz.
Cuatro secciones del género se encuentran en Colombia: s A Amomophyllum, sect. Massowia, sect. Dysspathiphyllum
y sect. Spathiphyllum. Cinco especies se conocen para la Amazonia y 11 aparecen ampliamente distribuidas en América

tral.

Colombia has the richest assemblage of Araceae working to complete a taxonomic revision of the
species (Croat, 1992) of any Neotropical country. genus for the Flora of Colombia, the preliminary

At least two genera, Anthurium Schott and Philo- results of which are presented below.
dendron Schott, exhibit their highest concentration Spathiphyllum includes 50 species that exhibit a
of taxa here. Despite the wealth of information re- tropical distribution; 47 species are restricted to the

garding Araceae in Colombia, few genera have Neotropics and the three remaining to the Philip-
been thoroughly studied. Here | present prelimi- pines and Indonesia (pers. obs.). Spathiphyllum is
nary data on the genus Spathiphyllum Schott in Co- easily distinguished from other genera in the family
lombia. Spathiphyllum is widely distributed in Co- by the combination of bisexual flowers (with peri-
lombia, occurring from sea level to 1300 m, but is anth), a persistent foliaceous spathe, the sheathing
most common in lowland forests, where it is closely portion of the petiole, which is 2 or more the total
associated with streams, often forming large colo- petiole length, inaperturate striate pollen, and ter-
nies. The taxonomy of the group is rather difficult, — restrial habit. Grayum (1990), Bogner and Nicolson
1991), and Mavo et al. (1997) all seem to agree
most recent revision of the genus (Bunting, 1960) that the genus appears most closely related to the
require further examination. The present author is Indomalesian Holochlamys Engl.

and the gross morphological characters used in the

p

' Lam grateful to Thomas B. Croat (MO) and Ric s Callejas (HUA), who carefully read the manuscript and provided
valuable suggestions. Data were gathered from fieldwork by the author in the M ao of C T MET complemented
with relevant literature апа. 1 85 ‘tions from all major RUE rbaria in the country (Ce OL. HUA, JAUM, MEDEL).
as well as the TROPICOS database. A visit to MO was possible thanks to an Ahern de nir e ie and financial
support for fieldwork in Antioquia and Chocó was provided by the Comité de Investigaci iones at the Universidad de
Antioqu uia

De parlamento de Biología, Universidad de Antioquia, AA. 1226 Medellin, Colombia. faca@matematicas.udea.
edu.co.

ANN. Missourt Bor. GARD. 91: 448-456. 2004.

Volume 91, Number 3

Cardona
Spathiphyllum in Colombia

Nine species of Spathiphyllum have been de-
scribed from the Neotropics since Bunting’s (1960)
revision of the genus. which treated 36 taxa: how-
ever, our knowledge of the ecology, reproductive
biology (Montalvo & Ackerman, 1986). evolution-
ary trends, and taxonomy of the group remains al-
most unchanged.

Spathiphyllum is known in Colombia by 18 spe-
cies. Despite intensive collecting in the area during
some taxa remain known
only from the type « Most
Spathiph yllum are cultivated, not only because they
are easily propagated, but also because of their at-
tractive, dark green, glossy foliage. in strong con-
trast with the pure white to greenish spathes and
spadix. Not surprisingly, many Colombian species
of Spathiphyllum were described from material col-
lected by European botanists in the 19th century

the last three decades.

collections. species of

searching for ornamental plants that could be in-
troduced to that continent. Unfortunately, due to the
vagueness of the horticultural trade in the past cen-
tury, data on specific localities is often poor or sim-
ply absent. Briefly | here provide data on geograph-
ical distribution and the state of knowledge for all

species of the genus known from Colombia.

Spathiphyllum Schott. Melet. Bot. 22. 1832.
ТҮ! Spathiphyllum lancaefolium (Jacq.)
Schott.

Terrestrial herb: rhizome creeping, often just be-
low the surface of the ground, the plant appearing
to be acaulescent; internodes short; roots emerging
through the petiole bases: leaves several. mostly
erect lo erect-spreading: petioles often fully
sheathed, with apical geniculum: blades oblong to
apex:

—

elliptic to narrowly elliptic, acuminate a
midrib sunken above,

mary lateral veins moderately numerous, extending

narrowly raised below: pri-
to the margins: interprimary veins and minor veins
nearly always present: higher-order veins trans-

verse-reticulate. Inflorescence solitary; peduncles

as long as or longer than leaves; spathe oblong-
elliptic to elliptic or obovate, acuminate at apex.
acute to obtuse or rounded and sometimes conspic-
uously decurrent at base, midrib and primary lat-
eral veins white or green but turning green in fruit:
spadix cylindrical, erect, shorter than spathe,
stipitate, rarely sessile, stipe often adnate in part
to the spathe; flowers bisexual, perigonate: tepals 4
to 6. arching over pistil and rarely fused into a ring:
stamens 4 to 6, free, filaments short, flattened: con-

nective slender: thecae. oblong-ellipsoid to ovoid,
dehiscing by longitudinal slit: pollen inaperturate,

ellipsoid to ellipsoid-oblong: gynoecium ovoid,

obovoid flask-shaped: ovary 3-

2- to 4-locular,

subeylindrical,
locular, rarely
per locule, anatropous to hemianatropous: placen-
ation axile; style conical and sometimes promi-

2, 4, 6, or 8

ovules

"

sometimes truncate: stigma 2- or

nently exserted,
3-lobed or subcapitate.
greenish: seeds oblong, elliptic to ovate or reniform.

Berries l- to 8-seeded.

pale yellow to brown, striate-verrucose; embryo ax-
ile, elongate, slightly curved: endosperm copious.

KEY TO THE SECTIONS OF SPATHIPHYLLUM IN COLOMBIA

la. Perianth segments totally connate

sect. Massowia

Ib. Pevianth segments free, al ee TN
2a. stil truncate to subtruncate or e and
scarce ds exceeding the perianth.

3a. Apex of the riii truncate to sub trun-
саіе 2. I. sect. Ming е
3b. Apex of the pistil blur cl.

Dy ЧЕТАТА (S. КОЛ
›. Pistil attenuate or co and exceeding
the perianth 6 бов

2 mica

Massowia (K. Koch)

I. as sect.
Phan. 3: 228. 1879

Engl.. in DC., Monogr.

TYPE: pus ow. cannaefolium (Dryand)
Schott.
KEY TO THE SPECIES OF SPATHIPHYLLUM SECT. MASSOWI4 IN

COLOMBIA

la. Primary lateral veins arising at 25—15°: Amazo-
nia : 1. S. cannifolium

Ib. Primary late ral veins arising at 50-055 Antio-
2 S laeve

quia and Chocó

l. ir cannifolium (Dryand.) Schott.
"cannaefolium" |.

Gen. Aroid. 1. 1853 [as
Pothos n 1 Dryand., Bot. Mag. 17. t.
603. 1803. TYPE: “Hort. Kew. 1790" (holo-

type. BM not seen).

Likely the most widespread species of the genus
in Colombia, Spathiphyllum cannifolium appears
restricted to the Amazon basin, where it is known
from practically all major tributaries of the Ama-
zonas. Caquetá, Vichada, Apaporis, and Guayabero
Rivers. A large gap in distribution exists, however,
in the central portion of the Colombian Orinoco and
Caquetá valleys, likely due to poor collecting in the
area

In Colombia, Spathiphyllum cannifolium occurs
at 200 to 1000 m elevation, in tropical wet forest
life zones, and flowers all year round.

Representative. specimens examined. COLOMBIA.
Amazonas: Me Igara-Parana, afluente del río TES

orreg. la Chorrera, J. Gasche 1137 (US); Santa Isabel.“
Pabon 684 (CO! AH, NY). Boyaea: carretera а

Annals of the
Missouri Botanical Garden

pal, quebrada Blanca, 7 km de Aguazul, С. Sastre 769
(US). Caqueta: 10 km al sur de Belen, 360 m, ene. 1974,
A. Gentry 9110 (MO); 13 km de florencia hacia El Don-
cello, J. Luteyn 4907 (MO, NY); 9 km al SW de Fragua,
A. Gentry 5730 (MO); Florencia, E. Perez 710 (COL, US);
San Vicente del Caguan, entre Campana y Puerto Majiña,
J. Betancur 2251 (HUA, MO); San Mini del Caguan,
Vda. el Recreo, Hato Varsovia, е La Sal, J. Be-
tancur 1619 (HUA, MO). Casa : Río Casanare, Es-
meralda, J. шиге asas 3844. (US S. 5 Lla-
no de San Martín, Triana 692 Meta:
Villavicencio, T Sprague ue (F, ae Hato Horizontes, J.
Blydenstein 1061 (COL, NY); 5 km de la via entre
Villavicencio y Granada, T ae 55530 (MO); llanos de
San Martin I Hoya del río Ariari, alrededores de la laguna
Aguasucia, R. Jaramillo 1136 (COL, US); sabanas de San
Juan de ABA. río Guejar, J. Ын 593 (COL, МО);

Guejar, E 1 2043 (COL, NY); Valle del Rio Guaya-
riba, 15 ) de Villavicencio, M. Grant 9942 (MO); Villa
de Сопсер i ave 14 km E de Villavicencio, J. Luteyn 4754
(MO, NY). Nariño: Canangucho, 162 km E de Pasto, ji
Espinosa 3049 (NY). Putumayo: entre Mocoa y Urcu
que, quebrada Obandoyaco, Ewan 16791 (MO, US); a.
tera Colombo—Ecuatoriana, Río San Miguel, entre los
afluentes Bermeja y Conejo, J. Cuatrecasas 11055 (US);
Mocoa & vic., А. Schultes 19044 (NY, US); Puerto Ospina,
Río Putumayo, J. Cuatrecasas 10861 (US); Umbria, C.
Klug 1663 (MO, NY). Vaupés: Mitu y alrededores, R.
Schultes 13975 (COL, NY, US); Río ариза, tributario
del río Apoporis, Caño Teemeeña, R. Schultes 17452 (US);
Rfo Vaupes, entre Mitu y Javarete, бш ed a, Е Se е
tes 19323 (GH, МО); Rio Vaupes, entre Mitu y Javaret
desembocadura de Querari, R. Schultes 19340 (US); Ri
veras del Río qus iege Alto, cerro el Varador,
d 2091 US). Vichada: 8 km al E de E

viotas, С. u 5169 (MO); borde del Río Vichada.
San José de Ocuné, J. Hermann 11052 (US).

~
©
=

Bot. Jahrb. 37

2. Spathiphyllum laeve Engl.,
ТҮ} Rica.

120. 1905.
dans les bois, Vallée Gissler, Пе Cocos, Paci-
fique," 18 June 1898, H. Pittier 12370 (holo-
type, B; isotype, US not seen).

Costa “Commune

Spathiphyllum laeve was until recently only
known from Isla de Cocos in Costa Rica. However,
a large number of collections of this taxon has been
made in the last decades from Nicaragua, Panama,
and Colombia, where it is restricted to the north-
eastern border adjacent to Panama in the states of
Antioquia and Chocó. Spathiphyllum laeve is rather
common in shaded sites in the understory of humid
forests on clay soils. It is the only known species
of Spathiphyllum sect. Massowia that occurs in Me-
soamerica and Colombia.

Spathiphyllum laeve grows from 0 to 900 m el-
evation in tropical wet forest life zones. Flowering
collections in Colombia have been made in January,
February, July, and October.

Representative specimens examined. COLOMBIA

Chocó: E side, Serranía del Darien, from Acandi, =

Guati river, A. Juncosa 607 (MO); Nuqui, correg. Terma-

les, J. Betancur 6016 (COL); Riosucio, Cerros del Cue chi-

llo, D. Cardenas 1348 (JAUM); trail from Rio Tigre base

camp up Serranía del Darien W of Ungfa, A. Gentry 15239
O

COSTA RICA. Alajuela: Res. Monte verde, Poco Sol 13
km 5 1 W. Haber 9349 (CR, i
Arenal by air, К. Liesner 15110 (MO); «
Balsa de San aa. М. Grayum 6352 (м )). Cocos Is-
land: Wafer Valley, L. Gomez 3286 (MO); near Wafer Bay,
К. Dressler 4465 (MO). Heredia: “Starkey woods,” across
river Puerto Viejo, R. Dressler 4679 (MO); А Баѕе of hills
to S of Río 55 opposite Chilama
5314 (MO). Puntarenas: along road жең |
& Panamerican border, 3 km N of turn-off Rincón,
Croat 79187 (MO)

T. B.

II. Spathiphyllum sect. Amomophyllum (E = )
Engl., in DC., Monogr. Phan. 3: 227.
TYPE: Spathiphyllum gardneri Schott.

THE SPECIES OF SPATHIPHYLLUM

AMOMOPHYLLUM IN COLOMBIA

SECT.

la. Leaf blade 3.5-9 times longer than wide.
2 Primary lateral veins arising at 11—30°.
Ja. Genic ш. 2-3 cm ia Lien
6.4 cm long -.... > quantae
3b. Ge — чп 0. 8-1 cm Jen. spadix
n lon $, “schomburgkii
5-709.

=

Primary 1 5 wal veins LT
4a. Leaf blade ovate-lanc colat base
obtuse; n ‚5. tenerum
4b. Leaf blade siccis elliptic to ob-
long; Amazonas or interandean val-
leys.

5а. 11 shorter than 25 cm;

onas |... 1. S. minor
5b. Pa tis sulle than 35 с m; inte-
ean valleys |... S. patinii

—

Leaf blade 2— 31 Че s longer than wide.
a. Primary lateral veins arising at n

-
=

8 en
Ob. P 1 lateral veins arising e —7(
Та. Petiole as long as the leaf blade.

E Leaf blade ovate тч,

— S. perezii
b. Leaf Майа oblane colate 1 to el-
и -oblong . s. floribundum
7b. 8 кез times re shan the
leaf blac
Оа. Сеп nic enliyi 2-3.5 кү eas
S Tilo 'ovirens
9b. Genie iba 0. -L7 7 cm lone.
10a. Spathe ie nt to the
peduncle 0.4—1.4 em —
). S. silvicola
10b. Spatie fos: or ine ee
uously decurre
E 5 pe

1. Spathiphyllum quindiuense Engl., Bot.
Jahrb. Syst. 37(1): 120. 1905. TYPE: Colom-
bia. Quindío: 1000 m, Triana 693 (holotype,
BM not seen).

Volume 91, Number 3
2004

rdona
Spathiphyllum in Colombia

Spathiphyllum quindiuense was first collected by
the Colombian botanist J. J. Triana from Quindío
(no further locality was specified). Additional col-
lections from Colombia were made by Castañeda in
1954 at Barrancabermeja along the Río Magdalena

and by F. C.

portion of Antioquia in the municipio of Nariño.

Lehmann in 1891 in the southeastern

Bunting (1960) reported the species as having been
collected in Panama by Seibert. Additional collec-
tions of S. quinduense from Puerto Berrio in the Río
Magdalena valley were made in 1990 by Н. Calle-
jas. who also collected the species in the tributaries
of the Río Cauca in the Central Cordillera in Co-
lombia.

Spathiphyllum quindiuense is known from tropi-
cal wet forest life zones at 200 to 1400 m elevation:
flowering possibly occurs all year round.
examined. COLOMBIA.
km de la vía Remedios

R. Callejas 5159

Represe ntative spec imens
Remedios, 14—17
Zaragoza, región del cerro —
(HUA); Amalfí, km 15—35, en la vía de las veredas Cho-
rritos—Los Monos, s 90 A (HUA . MO):

12, Bajo Cauca, entre las quebradas
rales. Callejas 227 (Н riño, Río San Pe-
dro. Lehmann 7590 (US Ei Puerto P rrio, vereda Alicante,
Finca Penjamo, | km al S de la finca, R. Callejas 9246
(HUA, NY): Puerto Berrio, vereda Bode gas, sitio San Juan
de Bedout, quebrada San Juan, R. Callejas 9341 (HUA):
San Carlos, corr. alto Samana, vereda el Silencio- Jardin.
R. Callejas 8523 (HUA, МО); San Luis. Río Dormilón.
Charco La Cascada, 5. Hoyés 93 (HUA); San Luis, Vereda
Manizales. a orillas del Río Dormilón, C. Orozco 616
(COL): a Trayecto Río Tiguí a Zaragoza. R. Calle-
jas 4621 (HUA).

Antioquia:

Caceres. Ca-

—

2. Spathiphyllum paa Schott, Oesterr.
Bot. Wochenbl. 57. TYPE: Venezue-
la. “Ist Coll. M. эы H. Н. Schomburgk

n. (holotype, K not seen).

Spathiphyllum schomburgkii was made a variety
of Spathiphyllum candolleanum by Engler (1879)
based on the nature of the pistil; however, after a
considerable examination of the pistil, Bunting
(1960) did not accept the varietal status.

Spathiphyllum schomburgkii was initially known
to be restricted to Mount Roraima in Venezuelan
territory; a careful examination of herbarium col-
lections at HUA revealed in Colombia at least two
disjunct populations of this taxon, both in north-
eastern. Colombia, one at the Magdalena valley
(state of Santander) and a second population at the
northern extreme of the Río Cauca canyon near the
town of Tarazá (Antioquia). The species appears to
be restricted to the margins of water streams in
shadowy places, and it can be recognized by the
low stature of the plants (0.35 m). the length of the
petiole (equal to or less than the lamina length),

and by the leaves narrowly elliptic. 4-6 times lon-
ger than wide

Spathiphyllum schomburgkii grows in tropical
100 to 500 m elevation.
in August

wel forest life zones at
Flowering collections have been made in
and September.

hepresentative €— bindet COLOMBIA.
DR wins Taraza, corr. E ‚ en camino a Barroblan-
. R. Callejas, S. Churchill et de 2397 (HUA, NY). San-
. Barrancabermeja, о Valley, betw.

Sogamoso & “Colorada Rivers, O. Haught 1367 (US

©
-
-

Jahrb.

3. do slo tenerum Engl., Bot.
120 05. TY Loreto: “Bo-

3 Л 4: Peru.
denpfl.. 1 » grunlich weeiss, Cerro de Ponasa.
1200 m." Feb. 1903. E. Ule 6851 (holotype,
В!: isotypes, G-DEL not seen. MG not seen).

Spathiphyllum tenerum. exhibits leaves that are
ovate-lanceolate (4 times longer than wide) and
secondary veins that diverge from the midvein in
angles of 70°. The species was first described by
Engler in 1905 from Cerro Ponasa in the province
of Loreto (Peru) at a rather unusually high elevation
the genus (1200 m).

known from the department of Amazonas in Colom-

fo A second collection is

bia but at much lower elevation (200 m).

Representative examined. COLOMBIA.
Amazonas: corr. Tarapaca, vereda El Porvenir, R. Lopez

et al. 4375 (COAH).

specimen

4. Spathiphyllum minor G. 5. Bunting. Mem.
New York Bot. Gard. 10(3): 31. 1960. TYPE:
Peru. Junín: Pichis Trail. Santa Rosa, 625—900
m. 6. 7 July 1929, E. Killip & A. Smith 26153
(holotype, US! isotype, NV).

Spathiphyllum minor, originally described by
Bunting (1960) from Junin (Peru), has been col-
lected in Colombia in the southern state of Ama-
zonas near the border with Peru. This species is
noted for its small size (0.3 m), the soft leaf texture,
and the rather short stipe.

Spathiphyllum minor is found at 200—300 m el-
evation in tropical wet forest. Flowering occurs in
January, March. July, and September.
specimens sum COLOMBIA.
Amazonas: Leticia, Río e ana, 3 c 114 (HUA): 750 de

larifio, G. Lozano, F Pat em V 2 8 618 (COL);
Leticia, кар de E et fa C alderon, R. Lopez, 7 85
Mazorra & Jose I. Marmoz 5889 (COAH); corr. Tarapaca,
R. Lopez, D. быш et al. 5022 (СОАН).

Representative

=

Spathiphyllum patinii (Hogg) N. E. Br., Gard.
Chron. 2: 783. 1878. Anthurium patini Hogg.
Gard. Year Book 123. 1875. TYPE: Colombia.

452

Annals of the
Missouri Botanical Garden

Antioquia: Gomez Plata, cuenca del río Porce,
hacienda Vegas de La Clara, 950 m.
6737'00"N, '00"W, ago. 2003, E Cardo-
na, К. Callejas et al. 1171 (neotype. designat-
ed here, HUA!; isotype, MO!).

75215

This species was first mentioned as Anthurium
patini in the Garden Year Book, by Hogg (1875) and
in Garden Chronicles by Masters (1875) without any
formal description but accompanied by a single il-
lustration. Afterward, N. E. Brown (1878), in clear
reference to Master's illustration, transferred A. pa-
tinii to the genus Spathiphyllum.

Since the original collection and Bunting's treat-
ment in 1960, specimens collected in Colombia
that agree. with the original description come from
the northern Magdalena valley in Antioquia near

the municipios of San Luis and San Carlos, where
the plants grow on rocky granitic outcrops. It is
worth noting that this region includes many endem-

c species of angiosperms first described in Europe
from horticultural catalogs. In fact, the area of San
Carlos was very much traveled in the 19th century
by European plant collectors, as it was the route
for entering Antioquia from the Río Magdalena. At
the present time, Spathiphyllum patinii seems to be
restricted to a narrow corridor in the Magdalena
valley and to a disjunct population in the Río Ano-
rí, a tributary of the Río Cauca in Antioquia.

Spathiphyllum patinii ranges from ЗОО to 1400 m
elevation in tropical wet forest and premontane wet
forest life zones. Flowering collections have been
made in most parts of the year.

pde specimens examined. COLOMBIA,‏ را
J. S. Mutis 1123 (MA, US). Antioquia: “Río‏ ,1760-1808
Claro, nie hwy. between Pto. Triunfo and Medellin.” 7.‏
Croat 56547‏

A): Puerto Berrio, La Car-
lota, quebrada El Vapor, А Cardona, A. Idarraga & J.
Benavides 1067 (HUA).

~
ج‎
=
=
=
к
2
^
>
~
22
е
ч zx
M
Rn
>
2
~
“2
>
%
м
~
~
D

6. Spathiphyllum kalbreyeri C. S. Bunting,
Mem. New York Bot. Gard. 3: 21, f. 5. 1960.
TYPE: Colombia. Rastrojas, 3000 ft., 15 Feb.
1880, W. Kalbreyer 1413 (holotype. K not
seen).

Since the original collections of Spathiphyllum
kalbreyeri, six collections have been made, two by
Hutchison in 1905 and O. Haught in 1936, and

four by the author in Antioquia. Spathiphyllum kal-

breyeri is known in Colombia from the Río Mag-

dalena valley at 100 to 500 m elevation in tropica
wet forest life zones.
Representative specimens examined. COLOMBIA.

Santander: vic. Barranc 5 Magdalena valley.
Carare Riv alt. 100—500 m, 1 July

etw. Sogam <
1936, 0. 7 8 1894 (US). Caldas: La Dorada, río de
la Miel, Hutchison 3194 (US). Antioquia: Maceo, Vereda

Jarbara, que 'bradas e sol y Alicante, V Car-
HUA): Puerto Berrio, La Car-
Е абий, A. Idarre

Santa |
dona & Carlos Lopez 1085
lota, quebrada El Vap or,
Benavides 1067 (HUA): a,
quebrada Puri, V. Cardona, p Callej as et al. 1049 (HU. ш
Valdivia, corregimiento Puerto Valli 1 cuenca del ri
Pesc ^e F. Cardona, R. Callejas & Carolina Robles 1078
(HUA

7. Spathiphyllum perezii C. S. Bunting, Acta
Bot. Venez. 10: 321. 1975. TYPE: Venezuela.
Mérida: carretera El Vigia-San Cristóbal de
Táchira, 9 km al suroeste del Vigia, entre el
Vigia y el Quince, en barranca silvestre, alt.
ca. 125 m, 3 Oct. 1967, G. S. Bunting 2405
(holotype, MY not seen).

Spathiphyllum perezii is here reported as new to
Colombia. The tvpe of this species comes from the
state of Mérida in Venezuela, collected by Bunting
in 1907.
Ramirez in 1987 and Grayum in 1986, both in the
Antioquia department near the Magdalena valley.

This taxon was first found in Colombia by

Spathiphyllum perezii ranges from 500 to 1500
m elevation in tropical wet forest life zones. Flow-
ering collections in Colombia have been made in
May, July. and September.

Representative specimens. examined. COLOMBIA.
San Luis, quebrada la Cristal ina, J. Ramírez
‚ MO); San û arlos, “primary forest qud
brada |: а Note, tributary to Punchiná reservoir, Río Gu:
tape,” M. Grayum 7628 (MO ).

8. Spathiphyllum floribundum (Linden & An-
dré) N. E. Br., Gard. Chron. 2: 783. 1878. An-
thurium Joribundum Linden & André, Ill.
Hort. 22, t. 159. 187. TYPE: Colombia. Anti-
oquia: San "Carlos, correg. El Jordan, vda. Jua-
nes, 230 m. Mar. 1988, L. Albert 8324 (neo-
type, designated here, HUA!; isotypes, MO!,

This species was first mentioned as Anthurium

floribundum in EMlustration Horticole by Linden

and André (1874). In Colombia many populations
of Spathiphyllum floribundum occur in the Cauca
valley in northern Antioquia and Rio Magdalena
valley, where it appears to be a rather common el-
ement of forest streams. It is sympatric with S. ful-

~
~

irens.
Spathiphyllum floribundum grows in tropical rain

Volume 91, Number 3

Cardona 453

Spathiphyllum in Colombia

forest life zones. from 200 to 1500 m elevation.
Flowering collections have been made throughout
the year.

COLOMBIA.
00

Representative specimens B

5 San Carlos. lake Punchina, A. Brant 1€
(HUA, MO, US): Amalfi, near Salazar, J. MacDougal 3992
(МО); 7 911 sitios Zalazar у Marengo, via Vetilla Fra-

guas, R. Callejas 9146 (HUA, NY): Anori, El Río y Bra-
эзне то, R. Callejas 8715 (HUA, MO, NY): San Carlos.
ca. 1.5 km from presa Punchina, M. rayan 7613 (MO):
San e corr. Alto Samana “Vda. Miraflores.” oo
da Miranda, К. Гена 2076 (HUA, MO, NY); San Car-
los. ISA hydroelectric dam reservoir. G. Mc Бегай 13336
(МО); San Luis “Quebrada la Cristalina.” J. Ramirez 1926
is, Cañón del Rio Claro, A. Cogollo
: San Luis. Piedra de D.
и . MO, NY): San Luis, río p Norte.
R. Callejas 4083 (Hl A, MO); San Luis, sector río Samana.
J. Hernandez 187 (HUA. NY): San Luis, Vda. la Josefina,
camino a Palmita, 5. Hoyos 469 (JAUM, МО); San Luis.
Vda. las Confusas, D. Cardenas 2669 (JAUM. MO): Ta-
E Callejas 2411 (HUA, MO): Río

=
=
p

Castrillon.

raza, correg. El Doce,

Nuz. Lehmann 7758 (F. US); Sabaleta, Le ЖО 7757 (F).
Boyacá: El ho, А. Law = 696 S). Cal-
das: Rio Samana, Caldas, A. Barkley о. rs Or-

doba: Tierralta. quebrada afluente del Río Simi. R. Ber-
nal 1191 (COL. MO). Cundinamarca: Paime. Bro.
Ariste- Joseph A924 (US). Santander: Magdalena Valley.
C ampo Capote, A. Gentry 20037 (MC Barrancaber-
a. betw. Sogamoso & Colorado rivers, O. Haught 1386

ej

)); vic.

meja

(US)

9. Spathiphyllum fulvovirens Schott, Oesterr.
Bot. Z. 8: 179. 1858. TYPE: Panama. Bocas
del Toro: vicinity of Chiriquí Lagoon, fish

Creek, 9 Apr. 1941, H. von Wedel 2198 (neo-
type, designated by G. S. Bunting (1960: 27).
GH not seen; isotypes, F not seen, MO!).

Common in Costa Rica and Panama, Spathiphy-
llum fulvovirens is also known from Colombia,
where it occurs in the northern portion of the Río
Magdalena valley, along the Pacific in Chocó and
Valle del Cauca and in the Amazonian states of
Caquetá and Putumayo. Bunting (1960
that the disjunct population in Colombia differs
from those in Central America in having narrower
leaf blades. Since his treatment, collections of this
species by Croat from Valle department and Cár-
denas in Pto. Berrio not only confirm Bunting’s ob-

servation. but also seem to indicate a disjunct dis-

indicated

—

tribution pattern for the Species.
Spathiphyllum fulvovirens in Colombia occurs at
200 to 1100 m elevation in tropical rain florest and

tropical wet forest life zones.

Representative specimens examined. COLOMBIA.
Antioquia: Puerto Nare, vda. Serranias, D. ardenas
3018 (] ); Тагала, corr. el Doce, Vda. Barroblanco

Amalfi, 8—15

quebrada Puri, R. Callejas 3627 (HUA);
de Amalfi a Rumazón, sitios Salazar y la Playa, J. Betan-

ud A);

2 787 (HUA); San Luis, Parque Ecológico El Castellon,
Alzate 1 7 (HUA): San Luis, Vda. zal
Turbo, carr. tapon del Darié

36. J. Brand 795 (JAU

Manizales, KR. €
én. р Rio

M. MO):

Leon- e 1

‘Iva veranera cerca de P en el valle del Río Me-
dellín. W. Hodge 6870 (US). Caquetá: 13 km SE de Mo-
relia along iy to Río Pescado (SW of Florencia). “

О). Chocó: Río Truando, J. Duke 13307
Duke 11219
W de
Putumayo:

Davidse 5680
(NY): rain c on hill N of alto Curiche, J. 7
se del Palmar y Novita,
T. Croat 56646 (MO).
Plo. Porvenir, se aras higrofilica del Río Putumayo, arriba
de Puerto Ospina, J. Cuatrecasas 10665 (COL). Santan-
der: vic. к 'abermeja, Magdalena Valley. betw. So-
gamoso & Carare Rivers, КЭ др; reek, O. Haught 1895
(US). Valle del Сын? from Queremal to Buenaventura,
along Río Ningaño, J. Croat 79724 (МО).

10. жылш M one: Duque R. A. Baker, Phyto-
logia 33: 448. 1976. TYPE: Costa Rica. Pun-
larenas: canton d de forest near Esquinas
Exp. study area betw. Río Esquinas € Palmar
de Osa, 200 ft., 3 Oct. 1967, P. H. Allen 5538
(holotype, Fl: isotypes, CRI, ТАР not seen, US
not seen),

Spathiphyllum silvicola is quite similar to S. laeve
in laminar shape and general appearance. Both
species can be distinguished rather easily, however,
by the apically free perianth segments of 5. silvicola
that are not united as in S. laeve.

Spathiphyllum silvicola ranges from the Chocó
lowlands along the northern Pacific Coast in Colom-
bia to the province of Puntarenas in Costa Rica.

Spathiphyllum silvicola grows in tropical rain for-
est and tropical wet forest life zones at 20 to 500
m elevation. Flowering collections have been made
in January, February, July, September, October, and
December.

COLA

specimens examine d.c

carr. Tapon

dre e Ies A.
Antioquia: Turbo, 3
Brand 795 (J. er" Corr. Lo
teria 3500 (JAUM. MO). Chocó: Parque N
Katios, zona del alto del а Guillermina, S. Zuluaga 1113

OL).

~

nother species in section Amomophyllum, Spa-
mom neblinae, is reported as occurring in Co-
lombia (Bunting, 1960). However, after examining
the collection of Schultes & Cabrera 15824 (MO),
I am convinced that it has to be referred to a new
species, at least based on its decurrent spathe and
short stipe, but more collections are needed to con-
firm it as such. The Schultes & Cabrera collection
was made in 1952 near the Miriti-Parana River, a
tributary of the Río Caquetá.

III. Spathiphyllum sect. Dysspathiphyllum
Engl. Pflanzenreich 4: 120. 1908. TYPE
Spathiphyllum humboldtii Schott.

454

Annals of the
Missouri Botanical Garden

Spathiphyllum sect. Dysspathiphyllum includes
the single species S. humboldtii, which has the dis-
tinctive feature of a blunt pistil apex.

l. epis iem humboldtii Schott, Aroideae

1: 2. . TYPE: “Surinam.” А W. Hostmann
1154 ide) designated by Bunting (1960:
33), K not seen: isotypes, BM not seen, G-
DEL!, U not seen).

—
—

The only species of section Dysspathiphyllum,
Spathiphyllum humboldtii is widespread in eastern
Amazonia and northeastern South America, where
it occurs from Surinam through Venezuela, French
Guiana, Brazil, Ecuador, and Peru. In Colombia, it
has been collected at Tuparro in the eastern part
of the country.

Spathiphyllum humboldtii in Colombia grows at
100 to 300 m elevation in tropical wet forest life
zones. Flowering collections have been made i
March.

Representative specimens examined. COLOMBIA. Vi-
chada: territorio faunístico del Tuparro, 4 km NW of the
headwaters x caño Peinillas, 160 m. Mar. 1980, P. Vin-
celli 1280 (COL, MO).

IV. Spathiphyllum sect. Spathiphyllum Bun-
ting, Mem. New York Bot. Gard. 10: 34. 1960.
TYPE: Spathiphyllum lancaefolium (Jacq.)
Schott.

KEY TO THE PECIES
SPATHIPHYLLUM IN Es OLOMBIA

Leaf blade 1.5-2 times longer than wide.
2a. Base obtuse or rounded . S. grandifolium
2b. Base acute 8. friedrichsthalii
Leaf blade 2.5-3 times longer ie wide.
Ja. Pistil exceeding the perianth by 0.3-0.4 cm,
cylindrical and rounded at 95 A SR |
S. fredrchsthali
Р йй & ехсее ding ihe: perianth 9 0. 1-0.2
attenuate-conic
4a. Leaf blade
"sd obtuse :

OF SPATHIPHYLLUM SECT.

la.

—

= ‘eolate, acute or some
A tue anum
. Leaf blade iri lance late or elliptic-
oblong, rounded, truncate or obtuse a
the base.
5a. Peduncle 1.4—1.7 times longer tha
the petiole А Ин бш
5b. Peduncle 0.6-1.1 times longe r than
the. petiole

the bi ase

=

S. phryniifolium

1. Spathiphyllum grandifolium Engl., Bot.
Jahrb. Syst. 37: 119. 1905. TYPE: Colombia.
Narifio: "auf dem Boden in dichten Regen-
wüldern bei Altaquer an den rei dd
qe Cordilleren von Pasto, 1000 m." 12 Mai

81

V. C. Lehmann 563 (holotype, B!).

This species was known until 1988 only from the
type locality in the Cordillera Occidental in Nariño
Department, where it was collected by the German
orchid and gold mining entreprenuer F. C. Leh-
mann in 1881. Working in Nariño during 1988, B.
Hammel collected this species once again, and in
1996 Silverstone-Sopkin extended its range of dis-
tribution to Risaralda along the
in northwestern Colombia.

Spathiphyllum grandifolium ranges from 900 to
1000 m elevation in tropical wet forest life zones.
Flowering collections have been made in March,
May, November, and December.

Cordillera Central

specimens TE COI .OMBIA. Na-‏ ا
rino: via El Espino—Tumaco, 30 km W de Ricaurte, El‏
Mirador, һпса Senta Lucia, B. Hammel 17181 (MO). Ri-‏

saralda: Hacienda Alejandria, km 6 carr. Virginia—Cerri-

to, valle del Río Cauca, P venisse p (CUVC, MO),
dic. 1995, P. Silverstone 7441 (CL О)
2. Spathiphyllum friedrichsthalii Schott, Aroi-

deae 1: 2. 1853. TYPE: Costa Rica. Limón:
"in Gynaerium sagittatum thickets along Río
Reventazón below farmhouse, Finca Castilla,"
30 m, 27 July 1936, C. W. Dodge & V. F. Goer-
ger 9414 (neotype, designated by Bunting
(1960: 35), К; isotype, MO not seen).

Engler described three varieties, two in 1879
(var. angustifolium and var. latifolium) and one in
1907 (var. brevifolium); however, these could be
geographical variations of the same species.

Spathiphyllum friedrichsthalii is the most wide-
spread of the four species known in Colombia from
section Spathiphyllum. It occurs in the Chocó re-
gion from the Darién in the north to the Colombian
border with Ecuador in the south. The species often
grows in large populations along streams and was
the subject of reproductive biology studies (Mon-
talvo & Ackerman, 1986). This species has been
introduced in the local horticultural market in Co-
lombia and is often seen as a house plant.

Spathiphyllum | friedrichsthalii is known from
tropical rain forest and tropical wet forest life zones.
Flowering collections have been made throughout
the year.

Representative specimens examined. COLOMBIA.
Antioquia: 18 km al sur de C оа М. Palacio 104
ЖУ MO, NY): ea 23-27

Callejas 9712 (HUA); near е > e
F Uraba, entre Mutata y

de = higorodo,
of Turbo,
a 'avarando-

ito, L. Uribe 2038 (COL, Villa Arte aga, C. Brahe
18C701 (US). Cauca: costa del Pacífico, Río Micay, Noa-

ш; J. Cuatrecasas 14217 (US).
шро. across river from Yuto, A. Gentr

a de Quibdo, J. Araque 19CH049 (US); Anda-

goya, Killip 35076 (US); Baudo, river Baudo, quebrada

Volume 91, Number 3
2004

Cardona 455
Spathiphyllum in Colombia

Majagual, H. Fuchs 1501 (US): camino entre Playas de
Oro y Tado, T. Croat 80763 (MO); carr. Istmina, 10 km
antes de Yuto, J. Santa 278 (HUA); en del río San
. Rio ais alrededores de Noanamá, E. Forero
A); Jurubidá, playa Pefias Blancas. que-
та А. Gomez 316 (НОА); Riosucio,
cerros del cuchillo, D. Cardenas 1386 (JAUM, MO); Pi-
zarro, carr. Pepe-Berrecul km 21, J. Espina 1937 (Chocó,
MO); Riosucio, cerros del cuchillo, D. Cardenas 1895
(JAUM, MO): Río Atrato, 2-5 hours below Río Sucio.
above Loma Teguerre, J. 55 11003 (US); Rio Serrano,
4—6 km arriba de ктт E. Forero 1388 (COL, МО);
Rio Truando, Schott 3 (NY); Trocha Utria al Valle, Costa
Pacífica, A. Fernandez 273 (COL, US). Córdoba: Dagua
Valley, Killip 5034 (NY, US). Nariño: Isla de Gallos, Pa-
cífico, Ё. san al 9 (U S); Rives du Río Mira, K. Lan-
yo 2 (US). Valle: Córdoba, Killip 33397 (US): Río Ca-
lima, La Trojita, J. Cuatrecasas c (US); Río Dagua,
Buenaventura, Le mann 5361 (NY); Río Raposo. dnm
field station, M. Bristol 700 (US); Sabaletas, km 29,
from Buenaventura to Cali, Killip 38859 (US

w

Spathiphyllum zetekianum Standl., Ann.
Bot. Gard. 27: 267. 1940. TYPE:
Panama. Barro Colorado island, canal zone,
July 1931, D. E. Starry 27 (holotype,
F-0512511).

Missouri

F, photo

Spathiphyllum zetekianum is found along the
western slopes of the Western Cordillera to the Pa-
cific lowlands of Chocó and neighboring Panama.
As with many other species of the genus, this ap-
pears to be restricted to the forest interior and as-
sociated with sandy or clay soils. It grows at O to
600 m elevation in tropical wet forest. Flowering
collections have been made in January, April, and
July.

specimens examined. COLOMBIA.
corr. Sapzurro, MEDEL 100 (MEDEL):

Representative
Acandi,

Nuqui, Corr. Arusí, est. biol. El Amargal, Jorge Jacome
314 (COL. HUA); Unguía, resguardo de Arquía, Giraldo.

Izquierdo & Pinto 45GIP (COL); Carmen de Atrato, carr.
entre el Carmen y Quibdo, F Cardona, R. Callejas et al.
1018 (HUA).

4. Spathiphyllum lancaefolium (Jacq.) Schott,

Melet. Bot. 22. 1832. Dracontium lanceaefo-
Coll. Nom. Broth. 4: 118. TY

Pl. Rar. 3: pl. 612 (1786-1793).

lium Jacq.,
Jacquin, Ic.

Spathiphyllum lancaefolium is likely the most
common and locally abundant species of the genus
occurring in the mid and upper Magdalena valley
of Colombia. but its presence in Colombia re-
mained undetected since it was first described by
Engler and Krause from neighboring Venezuela in

1908.
heights of almost 2 m and are a frequent component

Individual plants of this species attain

of the forest interior, in areas either commonly or

occasionally flooded. The species grows at 100 to

600 m elevation in tropical wet forest life zones.
Flowering collections have been made from July to
October.

Representative specimens examined. COLOMBIA,
Antioquia: Puerto Berrio, сайо a 4 km de San Juan de
3edout, en la via a Yondo, V. ah & R. Calleias 1112
(HUA): San Luis, cañon del río Claro, К Cardona et al.
1189 (HUA); San Luis, alrededores de la Vereda Chorro
de Oro, A. Cogollo et al. 4592 (JAUM). Caldas: Norcasia,
proyecto hidroeléctrico е i т E 6535 (HU il
Cundinamarca: Capar H. ча B. 7676 (COI
Quindio: La balsa, ue ans to › Toc he, 1844, ads
s.n. (MO). Santander: Cimitarra, 5 km despues de cruzar
el puente sobre el Río Magdalena desde Puerto Berrio,
hacienda El Bosque, F Cardona & Carlos Lopez 1090
TUA); ew potrero quito, J. Perez et al. 1096
(HUA. JAUM). Tolima: Mariquita, res.
mun., . Pie 17 (COL); Venadillo, ds "an Кайыын.
Je 188 E 31 (COL); Venadillo, Vda. Berlina, J. Idrobo
10765

—
®
ES

bosc jue de

—

5. Spathiphyllum phryniifolium Schott. Oesterr.
Bot. Wochenbl. 7(20): 159. 1857. TYPE: Pan-
ama. mouth of

1850, A.

“Chagres, Isthmus of Panama,”
the Río Chagres, canal zone. Jan.
Fendler 425 (holotype, K not seen).

Spathiphyllum phrynüfolium is known from Pan-
ama, Costa Rica, and Colombia. In Colombia it has
been collected (1976) in the northwestern portion
of the Chocó region along the border with Panama

by E.

department of Antioquia near Chocó, by Т. Croat.

Forero, and more recently (1990) in Salgar.

Spathiphyllum phryniifolium grows at 50 to 100 m
elevation in tropical rain forest and tropical wet
forest life zones. Flowering collections have been
made in February, March, November, and Decem-
ber.

Representative examined. COLOMBIA.
Chocó: Acandí, Unguia y alrededores, E. Forero 1986
(COL). Antioquia: Salgar, J. Croat 69892 (MO).

specimens

DISCUSSION

While collecting Spathiphyllum in Colombia, one
soon discovers that a strong ecological component
exists in species distribution, where substrate pref-
erences along watersheds are specific for many spe-
cies. Some species of Spathiphyllum prefer shady
sites and soils with sandy substrates along water-
courses (cf. S. floribundum, S. friedrichsthalii, S
cannifolium) that are not subject to periodical
flooding. On the other hand, species like S. patinii
prefer the exposed rock crevices along streams.
Spathiphyllum quindiuense prefers rocks on stream-
beds in fully exposed sites where the rhizomes are
always fully covered by wate

The genus Spathiphyllum exhibits distinct. pat-

456

Annals of the
Missouri Botanical Garden

terns of distribution in Colombia, which can be
summarized as follows:

It is evident that a considerable number of spe-
cies in the genus occur in or are restricted to the
Magdalena valley (9), and that fewer species (6) are
known from the Chocó region or Amazonia (5).

Nine species are known from the Magdalena val-
ley, none of which is endemic; five of these species
(S. floribundum, S. quindiuense, S. kalbreyeri, S. pa-
ипи, and S. fulvovirens) are known also from Pan-
ama (D'Arcy, 1987a, b). Spathiphyllum lancaefo-
lium, S. schomburgkii, and S. perezii occur also in
Venezuela, and S. floribundum, S. fulvovirens, and
5. quindiuense have disjunct populations in Ecua-
dor, Peru, and Panama.

Spathiphyllum humboldtii from the east of Co-
lombia has been collected Peru and Ecuador
(Croat, 1999; Vásquez, 1997).

For southeastern Colombia, in the Amazonian
basin, Spathiphyllum cannifolium exhibits a wide-
spread distribution and is by far the most common
species in that region. Other species such as S.
minor and S. tenerum are present in that region but
with one or few collections.

The genus Spathiphyllum is not documented as
very diverse in the Chocó Biogeographical Region,
with only six species known from the area. Spath-
iphyllum friedrichsthalii is widespread in Chocó,
while S. grandifolium, S. fulvovirens, and S.
phryniifolium are known from one or few localities.

Bunting (1960) documented the occurrence of 12
species of Spathiphyllum in Colombia (four exclud-
ed here: 5. neblinae, S. juninense, S. lechlerianum,
and S. kochii).
across four sections in Spathiphyllum: S. humboldtii
(sect. Dysspathiphyllum); S. phryniifolium, S. lan-
caefolium, S. zetekianum (sect. Spathiphyllum): S.

"

minor, S. perezii, S.

Here I report 10 additional taxa

U

schomburgkii, 5

. silvicola, S.

tenerum (sect.

Massowia).
Spathiphyllum is almost completely absent north

Amomophyllum); and S. laeve (sect.

of the Andes in Colombia; no species of Spathiphy-
llum are known from the Caribbean coast of any
states and, more surprisingly, none has been col-
lected from the Sierra Nevada de Santa Marta, an
area with lowland forests and extensive and rich
river systems. Also noteworthy is the paucity of
species documented for the Chocó, an area rich in
Anthurium and other Araceae, but evidently poor
for Spathiphyllum. The Andean region itself is by
far the richest part of Colombia in species of Spat-
hiphyllum in the interandean valleys.

It is likely that insufficient collecting in Ama-
zonian Colombia and even in the Sierra Nevada de
Santa Marta may explain the low number of Spat-
hiphyllum species in these areas; however, Chocó
and the Pacific coast in general had been inten-
sively collected at least for Araceae by Croat and
for general flora by Gentry. It is expected that fur-
ther fieldwork may corroborate the preliminary re-
sults presented here.

Spathiphyllum species occur along river banks,
on loose clay or sandy soils in shady areas. Such
habitats are more common in the interandean val-
leys below 1300 m than on the rocky river banks
of the Chocó region. More research on the ecology
of the species and more extensive collecting, nev-
ertheless, are necessary before a solid hypothesis
can be formulated to explain the distribution of the
genus in Colombia.

Literature Cited
Bogner, J. & D. Nicolson. 1991. A revised classification
of Araceae with dichotomous keys. Willdenowia 21: 45—

50.

Brown, N. E. 1878. Spathiphyllum patinii. Gard. Chron.
2: 783.

Bunting, G. S. 1960. A revision of Spathiphyllum (Ara-
ү, Mem. к. 17 Bot. Gard. 1003): 1—53.

Croat, T. B. 1992. Species ie of
bie л preliminary survey.

Araceae in Colom-
Ann. Missouri Bot. Gard. 79

3
N

. 1999, Araceae. In: P. Jørgensen & S. Yáñez (ed-
itors), и of the Vase d dye of Ecuador. Mo-
e Syst. Bot. Missouri Bot. Gard. 75: 227—246.

VAr W 0. 1987a. Flora of Panam, с hec klist. Monogr.
Svat Bot. Missouri Bot. Gard.
. 1987b. llora E ча Ее
Bot. Missouri Bot. rd. 18: 1-67
fies 1905. 1 tenerum. Bot. Jahrb. Syst. 37:
120.

a > Monogr, Syst.
70.

~

Grayum, M.
ceae. Ann.

Hogg, R. 1875
123.

1990. Evolution and phylogeny of the Ara-
Lage toe ot. Gard. 77: 628-697.
Anthurium patini. Gard. Year Book,

Masters, M. 1875. Anthurium seg Gard. 1 575 2: 783.
ayo, S., J. Bogner & P. Bo neck

Araceae. Royal Botanical das

ces A. & D. Ackerman. 1986. n dae pollinator
effectiveness and evolution of floral traits in 5
pe улей (Araceae). Amer. J. Bot. 73: 1665
167

oe R.

‘he Genera of

1997. Flórula de las Reservas Biológicas de
m Soa Monogr. Syst. Bot. Missouri Bot.
104.

Gard.

Note added in proof

Since “ie manuscript was submitted in 1999 fieldwork
in several areas of Colombia has revealed the presence of
other species of Sp athiphyllum, 9 of which are taxonomic
novelties and are not included here. The total aeri of
taxa for the country is now estimated to be 27 spec

ARACEAE FROM CENTRAL Eduardo G. Goncalves?
BRAZIL: COMMENTS ON
THEIR DIVERSITY AND

BIOGEOGRAPHY!

ABSTRACT

Current knowledge about the diversity and biogeography of aroid taxa from central B razil is here presented and
discussed. For practical reasons, the study area was limited to the Cerrado phytogeographic 3 In all, 18 genera
and 64 фоне of Araceae were found naturally occurring in the studied area. The genera found were: Philodendron
: Anthurium (11), Xanthosoma (7), Dracontium (3), Monstera (3), Caladium (2). Dieffenbachi ia (2), Spathi-
carpa (2), Тырай (2). as well as Asterostigma, Gearum. Heteropsis, Pistia, Rhodospatha, Se ipn mi Spa uhiphyllum,
l кын» апа Zomicarpa (1 species each). The Jaccard similarity index between aroid flor the Cerrado province
and the two main contiguous forested provinces (Mata Atlántica and Amazonia) was т for both genera and
species. The values obtained show a closer similarity T species composition between the Cerrado and Amazonia (0. "d
than between the Cerrado and Mata Atlántica (0.088). However, the generic similarity with Mata Atlántica (0.591
higher than with Amazonia (0.414). Approximately 32% of the aroid species of central Brazil can be considered endemic
only genus known to be endemic to the Cerrado is Gearum

—

nee; the

to e Cerrado prov
Key we rds:

pia сае, io dicm Brazil, Cerrado. savanna.

In recent years, Brazilian ecosystems have been
intensively studied, and floristic inventories (espe-
cially at the family level) have flourished. However,
most published Floras concern Amazonia or areas
of the Atlantic coastal forest (Mata Atlantica). Only
a few studies dealt with areas of central Brazil
where the biodiversity still remains poorly known
or even unknown. This state seems even worse in
families (such as Araceae) that are known to be less
diverse in central Brazil than they are in other ar-
eas. Groups like these have been overlooked for a
long time.

Most of central Brazil lies inside the Cerrado
phytogeographic province, and this circumscription
of the Cerrado province establishes the scope of my
investigations (Fig. I). The Cerrado province is
characterized by middle-altitude uplands, usually
ranging from 300 to 1300 m, but occasionally from
sea level (Eiten. 1972

Kóppen's Aw category (rainy tropical), and there is

). The climate corresponds to

a well-marked dry season that lasts up to 5 months
(Kiten. 1994). The average rainfall ranges from 650
to 2000 mm/year (Assad, 1994).

of the Cerrado province is covered by cerrado veg-

The main portion

elation, a savanna-like formation that usually oc-

curs on very poor soils, and its аго diversity is
not immediately apparent. However. according to
Ribeiro and Walter (1998), approximately 15% of
the Cerrado province consists of differing vegeta-
tion types where aroids can be found, namely: gal-
[егу forests, seasonal marshes, hyperseasonal sa-
forests, limestone and

vannas, dry outcrops,

montane vegetation (campos rupestres). The aroid
flora in most of these areas is still poorly known.
and some recent studies have shown a surprising
number of new species (Gongalves, 1997, 2000a,
b. 2003a; Goncalves & Mayo, 2000; Sakuragui &
Mayo, 1997

—

MATERIALS AND METHODS

Most data shown here were obtained during the
initial and exploratory phase of the project “Bio-
diversidade do Bioma Cerrado.” The geographic
delimitation of the Cerrado phytogeographic prov-
ince follows the data compiled by Ribeiro and Wal-
ter (1998). Despite the fact that there are some dis-
junct areas of cerrado vegetation forming islands
within Amazonia as well as other phytogeographic
provinces, e.g., Caatinga province, only the central
contiguous cerrado area will be treated here. Field

This work was funded by grants from the project “Biodiversidade do Bioma Cerrado”
vork was conducted at the University о
Simon Mayo for important suggestions on the manuse ript. After the presentation p

DIFID). Part of this v
and FAPESP (99/02921-7). I thank

(E Weg овара 0

Herbarium UB. The author was funded by €

3rasilia.

this paper at the УШ International Aroid Conference, I updated this article in order to include recent advances in

ipid taxonomy and floristic knowledge
Jniversidade Católica de Brasíli:

Lote 1, EPTC, CEP 72030-170. ашны) DE, Bra

ANN. Missouni Bor.

; Cio de Ciências Biológicas, Prédio São Gaspar Bertoni, sala M-200, QS 7,
zil.

GARD. 91: 457—403. 2004.

458 Annals of the
Missouri Botanical Garden

4

——

— MÀ

[| DUO.
i i Р;
A
Le MM '

d a 4 at /

20%

Y

Figure 1. Central contiguous area of Cerrado phytogeographic province (adapted from Ribeiro & Walter, 1998).

trips were conducted from 1995 to 1999, mainly to compare the cerrado vegetation with other biomes
areas where aroid collections were scanty. Dried in Brazil, the preliminary checklist of Brazilian Ar-
specimens obtained from most herbaria inside the aceae (Mayo et al., 1996, available from the author
Cerrado province were also surveyed and mapped. upon request) was used together with the checklist
The final report (including maps for all taxa) is still compiled by Govaertz and Frodin (2002). The data
in preparation and should be published elsewhere set was critically updated using the literature pub-
(Goncalves, Proenga & Rosa, in prep.). In order to lished after the last checklist (Gongalves, 2003a, b,

Volume 91, Number 3
2004

Gonçalves 459

Araceae from Central Brazil

c; Gonçalves & Temponi, 2004) and recently col-
lected herbarium material. Comparisons between
the aroid flora of the Cerrado and other phytogeo-
graphic provinces were made using the Jaccard in-
1998).

was calculated considering species as well as gen-

dex of similarity (Morrone et al., The index

era.
RESULTS
THE CERRADO AS A MOSAIC OF FORMATIONS

A total of 18 genera and 64 species of Araceae
was found occurring in the Cerrado province. and
these are listed in Appendix 1. The most diverse
genus is Philodendron, with 23 species. followed
by Anthurium (11 species) and Xanthosoma (7 spe-
cies). Dracontium and Monstera have three species

each. Caladium, Dieffenbachia, Spathicarpa, and
Taccarum have two species each. All the remaining

genera (Asterostigma, Gearum, Heteropsis, Pistia,

Rhodospatha, Scaphispatha, Spathiphyllum, Uros-
patha, and Zomicarpa) are represented in the Cer-
rado province by only one species each.

Although usually treated as a phytogeographic
province, the Cerrado can be considered a mosaic
of different formations, each one influenced by dis-
tinet environmental conditions as well as different
paleoclimatic events. In order to present this com-
plex framework, I decided to discuss each forma-
tion separately.

Cerrado (sensu stricto). This can be considered
the “typical” structural type of the cerrado vege-
tation. It can be defined as a savanna woodland
with scattered contorted trees and a ground layer
of grasses, sedges, and occasional shrubs (Киеп,
1972). No species of Araceae were found growing
in pure forms of this structural type, perhaps be-
cause the soils usually have high quantities of toxic
1979).

This is considered a taller form of

aluminum (Goodland & Ferri,

Cerradáo.
the cerrado type, usually occurring on slightly rich-
er soils. Some terrestrial aroids can be found grow-
ing on these well-drained soils, mainly Taccarum
crassispathum E. G. Gong, Scaphispatha gracilis
Brongn. ex Schott, and a still undescribed Dracon-
tium. Climbers and hemiepiphytes are almost ab-
sent, except for the very occasional occurrence of
Philodendron wullshlaegelii Schott.

Hydromorphic formations. These formations in-
clude permanent marshes, seasonal marshes, and
hyperseasonal savannas. Permanent marshes have
standing water throughout the year, and aroids like
Urospatha sagittifolia (Rudge) Schott, Philodendron
uliginosum Mayo, and a still undescribed species
Dieffenbachia Seasonal

of there.

-

usually grow

marshes have water above the soil surface during
the rainy season, but it usually stays some centi-
meters below the soil surface during the dry season.
Xanthosoma striatipes (Kunth) Madison usually oc-
curs in this kind of marshy habitat. Hyperseasonal
savannas are characterized by the alternation of ex-
treme drought and flooding during the year (Sar-
miento, 1983). In these savannas, Gearum brasi-
liense N. E. Br. and Dracontium margaretae Bogner
can be found. Interestingly, both species from hy-

—

perseasonal savannas can be recognized by their

linear leaflets.
Gallery forests. These formations usually occur

along rivers and major streams. The gallery forests

ss

are usually treated as “corridors” of the Amazonian
forests and of Mata Atlântica that extend inside the
Cerrado province in a dendritic framework (Fer-

1998: Cabrera & Willink. 1973). Some ar-

vids growing in this habitat are hemiepiphytes.

nandes.

such as Philodendron guaraense E. G. Gong., Р.
lundii Warming, and P. mello-barretoanum G. M.
Barroso. The delicate climber P. guttiferum Kunth
is also common. Riparian aroids, e.g.. Spathiphyl-
lum gardneri Schott and Xanthosoma riparium E.
G. Gonc.. сап be found growing on river banks.
Although rheophytic aroids are not as common in
the Neotropics as in the paleotropics. one of the
few rheophytic species of Philodendron сап be
found in central Brazil. Philodendron flumineum К.
G. Gong. is common in rocks along fast-moving wa-
ter (Goncalves, 2000b). In fact, the vegetative con-
vergence between such species of Philodendron
and the Asian rheophytes аид Piptospatha

—

is overwhelming, such as creeping stems firmly at-
tached to the substrate and leathery leaves (lan-
ceolate or long-elliptic) with a rostrate apex.

Mesophytic forest. Mesophytic forests (also
known as dry forests) are usually found in restricted
areas with well-drained and rich soils. This for-
mation is often semideciduous (or even deciduous),
and tuberous Araceae are common, namely Xan-
thosoma plowmanii Bogner, X. syngoniifolium Rub-
sy, an undescribed tuberous Xanthosoma, Taccarum
crassispathum, Asterostigma cryptost ylum Bogner.
an undescribed Caladium, and Spathicarpa gard-
neri.

Limestone outcrops. These formations are usu-
ally rich in aroids, some of them growing directly
on exposed rock (e.g., Anthurium plowmanii Croat
and A. affine Schott). Other species are usually
found growing in humus-filled crevices, often in the
understory of deciduous forests. This group in—
cludes Taccarum crassispathum, T. weddellianum
Brongn. ex Schott, Spathicarpa gardneri, and Xan-

thosoma pentaphyllum (Vell.) Engl. All tuberous

Annals of the
Missouri Botanical Garden

30
m 25
E
9 20
a. |
Ф |
© 15
tæ
2
g 10
2
| a
0 "— | | N -— — 8
hs ge he ep me ff re
Life forms
Figure 2. Life forms of aroids from the Cerrado province: hs, hemie ا‎ 'andent; ge, geophytes; he, helophy-

tes; ep, epiphytes; me, mesophytes; ff, free-floating 9 F re, rheophyte

taxa lose their aerial parts during the dry season.
Meanwhile, species of Anthurium and Philodendron
remain evergreen throughout the year, and some-
times they are the only plants in the outcrops that
retain green leaves during the dry season.

Many species of the flora of these limestone out-
crops (and also from deciduous and semideciduous
mesophytic forest) follow the distribution pattern
stated by Prado and Gibbs (1993), i
mainly in three nodal areas (Caatinga, Missiones,

e., they occur

and Piedmont) with scattered occurrence in calcar-
eous-rich soils within the Cerrado province.
Campos rupestres. Within the Cerrado biogeo-
graphic province, two areas are usually considered
as “campos rupestres”: the Chapada dos Veadeiros
region, in northern Goiás, and the Espinhaco range
in the southeastern. portion of the province, in the
state of Minas Gerais. Some authors also include
the Chapada dos Guimaraes region in northwestern
Mato Grosso. Giulietti and Pirani (1988: 43) char-
acterized the campos rupestres of the Espinhaco
Range as usually “above 900 m, in association with
a high degree of outcropping and consequent re-
duction of soil depth." Basically the same condi-
tions occur at the Chapada dos Veadeiros, and some
components of the campo rupestre flora аге com-
mon to both areas (Giulietti & Pirani, 1988). How-
ever, the aroid flora of the campos rupestres of the
Espinhaco range are rich in endemic taxa (Sakur-
agui & Mayo, 1997; 2000), whereas no
species of Araceae can be considered endemic t

Sakuragui,

)

the campos rupestres of the Chapada dos Veadeiros.

In fact, if based only on the flora of Araceae, the
campos rupestres of the Espinhago range can be
considered an insular micro-province within the
Cerrado, Species like Philodendron biribirense Sak-
uragui & Mayo, P adamantinum Schott, and P. ci-
poense Sakuragui & Mayo are only found in the
Espinhaço range, and most of them are restricted
to high elevations. In contrast, the most conspicu-
ous aroid in the Chapada dos Veadeiros region is
Philodendron | wullshlaegelii, which also occurs
commonly outside of the campos rupestres at lower
elevations.

THE CERRADO PROVINCE
PHYTOGEOGRAPHIC

WITH RESPECT
PROVINCES

TO OTHER

The Cerrado is between two important, essen-
tially forested provinces: the Atlantic coastal forest
(Mata Atlántica) and Amazonia. In order to deter-
mine the relative importance of each one of these
forested provinces in the aroid flora of the Cerrado,

Jaccard’s index of similarity was calculated for spe-
cies and also for genera (Table 1). It is noteworthy
that the species similarity between the Cerrado
province and Amazonia is much higher than be-
tween Cerrado and Mata Atlántica (an index value
of 0.127 vs. 0.088, respectively). However, when
the similarity of genera is calculated, the situation
reverses with more genera being shared between
the Cerrado and Atlantic Coastal Forest (index val-
ue of 0.591) than between the Cerrado and Ama-
zonia (index value of 0.414)

Volume 91, Number 3
004

Gonçalves
Araceae from Central Brazil

4

Y
AS

.

| ж

Figure 3. Known occurrence of Gearum brasiliense М.

province (see Fig. 1).

It should be emphasized that the concept of Mata
Atlántica used here is broad, i.e., it also includes
the subdeciduous forests of southeastern Brazil as
well as those forests along the Paraná basin. Some
studies have shown that these formations can be
very distinct from the strictly coastal forests (Oliv-
eira-Filho & Ratter, 1995), but the available data
about the diversity of aroids do not offer such de-
gree of resolution.

Life forms. Тһе proportion of life forms that can
be found in the Cerrado province is summarized in
Figure 2. It is noteworthy that only 6 species (9.4%)
are known to be true epiphytes, and this is a very
low frequency when compared to other biomes in
Brazil such as Mata Atlántica and Amazonia. It is
also interesting to note that 14 (21.9%) of the spe-
cies found are geophytes and at least 19 (29.7%)
have a seasonally induced dormancy period. The
proportion of helophytes is also high (21.9%), but
only 4 species (6.2%) considered are true meso-
phytes.

Endemic taxa. Our results support that 35.9%
(23 species) of the aroids found are endemic to the
Cerrado phytogeographic province, namely Anthur-
ium megapetiolatum, Asterostigma cryptostylum,
Caladium tuberosum, Caladium sp. nov. [ined.].
Dieffenbachia sp. nov. [ined.]. Dracontium sp. nov.
[ined.]. Gearum brasiliense, Philodendron adaman-
tinum, P. biribirense, P. cipoense, P. dardanianum,

P. flumineum, P. guaraense, P. lundii, P. mayor, Р.

44
yr” D, r |
2 И Y 7

77

YY
fy

Br. (black area). Shaded area indicates the Cerrado

F
m

mello-barretoanum, P. rhizomatosum, P. uliginos-
um, P. venustifoliatum, Taccarum crassispathum,
Yanthosoma plowmanii, X. riparium, and Xantho-

soma sp. nov. [ined.]. The only genus endemic to

—

the Cerrado province seems to be Gearum (see its

distribution in Fig. 3).

DISCUSSION

Three separate events possibly have contributed
to the actual patterns of diversity and distribution
of aroids in central Brazil. They are: (1) the expan-
sion and subsequent contraction of the rain forest
during periods of less seasonality (as proposed by
Prance, 1982): (2) expansion and subsequent con-
traction of the dry forests (as proposed by Prado &
Gibbs. 1993) during periods with a more seasonal
climate: and (3) filtering effect of aroid taxa from
the Amazonian or Atlantic rain forest (Mata Atlán-
tica) that enter the Cerrado province by means of
riverine gallery forests, as proposed by Fernandes
1998). In this last instance, it is expected that the
axonomie diversity of these groups declines with
the distance from their “source” province. Studies

are ongoing in order to test this hypothesis.
Preliminary observations have shown that the
Cerrado province shares more species with Ama-
zonia than with Mata Atlantica. On the other hand,
more genera are shared between the Cerrado and
Mata Atlántica. The low similarity of genera be-

462

Annals of the
Missouri Botanical Garden

Table 1

cies of Araceae, between

Jaccard similarity index for genera and spe-
> Cerrado and the two main

— 2

forested provinces in Brazil. The number of genera and

species was based on Mayo et al. (1996) and Govaertz and

Frodin (2002).
Total Total
number number
of of Species Genera
species genera similarity similarity
Amazonia 184 23 0.127 0.414
Mata Atlántica 132 17 0.088 0.591

tween the Cerrado and Amazonia results from a
high number of genera that are known to be en-
demic to the Amazonian province, such as Allos-
chemone, Bognera, Ulearum, Zomicarpella (Mayo et
al., 1997), and Anaphyllopsis (Hay, 1988). Only the
aroid genus Dracontioides is known to be endemic
to Mata Atlántica.
Araceae of the Cerrado province is not negligible.
Approximately 35.9% of the species are endemic
to the Cerrado; some of them have very restricted
occurrence, e.g., Philodendron guaraense (Gongal-
ves, 1997). The one genus that can be considered

The level of endemism in the

endemic to the Cerrado is Gearum, which occurs
in hyperseasonal savannas, flooded gallery forests,
and eventually the cerradáo (Bogner & Goncalves,
1999).

The high frequency of tuberous aroids, as well
as the low frequency of epiphytes, seems to dem-
onstrate the importance of seasonality in the diver-
sity of Araceae in central Brazil. Tuberous plants
can remain leafless during the dry season.

It should be mentioned that the aroids of the
Cerrado province are among the most seriously
threatened in Brazil due to the fast expansion of
soybean cultivation as well as pastures, which are
destroying their native habitats. A more detailed
knowledge of their diversity may allow the estab-
lishment of strategies to warrant their conservation
as well as the maintenance of their genetic diver-
sity.

Literature Cited

Assad, E. D. 1994. Chuva nos Cerrados—Análise e Es-
pacializagáo. Embrapa-CPAC, Brasília

Bogner, J. & E. G. Goncalves. 1999, The genus Gearum
(Araceae). 5 ж 20—29.

Cabreira, А. & às
ma 'rica оа

e los

Villink. 1973. Biogeografía de
: cea Gene 0 de la Organización
dade Ame 'Ticanos, "lon.

Washingt
errado e of Brazil. Bot. Rev.

Eiten, G. . The e
38(2): : TE M.

— . Vegetacáo ni Cerrado. Pp. 17-73 in M. N.
Pinto ln Cerrado: Caracterização, ocupação e per-

spectivas. КЧ. Universidade de Brasflia, Brasília.

Fernandes, A. 1998. Fitogeografia Brasileira. Ed. Multi-
graf, Fort alea

Giulietti, A. M. & J. R. Pirani. 1988. Patterns of geograph-
ic кж from the E see inas G
and Bahia, Brazil. Pp. 71-120 i ‚ Vanzolini &
R. Heyer (editors), Pre DE fs a Workshop on Neo
tropical Distribution tà rns. Academia Brasileira de
Ciencias, Rio de Janeiro.
Goncalves, E. G. 1997. A new species of го
(Агас ic 2n central Brazil. Kew Bull. 52: 499-502.
Xanthosoma riparium (Arac eae a new
species a Goiás, razil. Novon 10: 2
————. 2000b. Two new species of Philodendron (Ara-

ceae) from central Brazil. Kew Bull. 55: 175-180.
2003a (“2002”). New aroid 13 from Brazil.

ideana 25: 10—35.

. 2003b (“2002”). New species and changing con-
cepts of Philodendron subgenus Meconostigma (Ara-
ceae). Aroideana 25: 2—15.

. 2003c. A new species and two new combinations
for the tribe Spathicarpeae (Araceae). Aroideana 26:
22-26

8
8 8

Aro-

é ‚ Mayo. 2000. Philodendron ee

m A new species from Brazil. Kew Bull.

483—44

E |. G. Temponi. 2004. А new е (Ага-

eae: Monsteroideae) from Brazil. Brittonia 56: 72—74.

Goodland, R. A. & M. С. Ferri. 1
rado. Aris ae Pau ilo.

yovaertz, R. . Frodin. 2002. World Checklist and
lin 4 ла ‘eae (and Acoraceae). Royal Botan-
le Gar rder ns,

Hay, A. 1988. О а пе » oe al genus of
Arace ‘eae: Lasie M Aroide la

9 кш чк 4 n

ares & C. S.

1979. Ecologia do Cer-

=
—

c

aa, C. M.

. Barros. 1996.
Checklist da Familia He ‘eae no p Unpublished
checklist.

Sakuragui, M. ГА A

1997.

p

‚ J. Bogner & P. C. Boyce. The Genera of
Araceae. Royal Botanic Саке “ns,

yinosa-Organista & J.

%
=

Morrone, J., D. S Llorente-Bous-
quets. 1998. Manual de Biogeografia Histórica. Ed.
Universidad Nacional Autónoma de México, México.
D.F

Oliveira-Filho,
origin of

A. T. & J. A. Ratter. 1995. A study of the

central Brazilian forests by the analysis of
plant species distribution patterns. Edinburgh J. Bot.
52: m 24.

Prado, E. & P. E. Gibbs. 1993. Patterns of species
UM in the dry seasonal je ud South Amer-
ica. 1 Bot. Gard. 80

Prance, ‚С. е ге Pan s: 5 vi 5 nce a wood y
TS 37-158 . T. Prance (editor), Bi-
ological Dive uns ation in the 1 9 5 Columbia Univ.

T

ress, New York
Ribeiro, J. F & B. M. T. Walter. 1998. Pus xcu do
Bioma Cerrado. Pp. 89-166 in S. M. Sano & S. P

Almeida (« y d Cerrado: Ambie nle e Flora. ЕМВК, "i
PA-CPAC, Brasília

Sakuragui, C. i 2000. Araceae of campos rupestres from
the E АА А un in Minas Gerais state, Brazil. Aro-
ideana 23:

—— & S. n e . 1997. Three new species of Phil-
odendron T Araceae ds Aen southeastern Brazil. Kew Bull,
52: 0734

Sarmiento, G.

1983. The savannas of tropical America.

Volume 91, Number 3

Goncalves 463

¢
Araceae from Central Brazil

Рр. 245-288 in К. Bourliére (editor), Ecosystems of the
World 13—Tropical Savannas. Elsevier, Amsterdam.

APPENDIX 1

Checklist of the Araceae occurring in the Cerrado phy-
togeographic province in Brazil. Asterisks (*) indicate taxa
that are considered endemic to the Cerrado.

А. croatii Madison; A. gracile (Budae)
А. megapetiolatum E.

A. е
. scandens (Aubl.
4. iced Schott

ın
A. Ane Scho
A, кен n Engl.:
Gone. + A. minarum Sakuragui &
P G. Don: A. plowmanii Croat: .
; A. sinuatum Benth. ex Schott;

d

i2
cryptostylum Bogner*

Cali

C. tuberosum (S. Moore) Bogner & Mayo*; C. sp.
[ined.]*
т 1c

). e D. sp. nov. [ined.]*
Pos ontium

J). margaretae Bogner:
*

nov.

ulei Krause; D. sp. nov.

G ана E. Br.*
Heterc

Н. oblongifolia Kunth
Monstera

М. adansonii Schott;

pre dE G. Gong. & Тилин

Donn. Sm.; /
Philodendron

P. adamantinum Engl.*; P. biribirense Sakuragui &

. dissecta (Schott) М. E. Br. ex
Go

Mayo*; P brandtianum Krause; Р. brevispathum Schott; P
ee 2 arroso; P. F^ nse Sakuragui &
May P. dardanianum Мауо*; P flumineum E. G.

бу + P. guaraense E. С. Gong V guttiferum r4
Р гае Kunth; P. lundii E. G. Cane. *: P mayo E.
Gonc.*; P. megalophyllum Schott: P. mollo- is
G. M. Ba rroso*; Pn minarum Engl.: P. rhizomatosum Sak-
"ыр & Мауо*; Р. solimoensense A. C. Smith; P. uleanum
Engl.: P. uliginosum Mayo*; P. ve тимоии Е. С.
. & Mayo*; P. wullschlaegelii Schot sp. nov.

Scaphispatha

. gra iii Brongn. ex Schott
Sparhicar arp

9 10 % Schott; S. hastifolia Hook.
d

о Schott

ко т

T. 5 G. Gong. *; T. weddellianum Brongn.
ex Schot
Urospat n

U. sagittifolia (Rudge) Schott
Xanthosoma

X. ا‎ (G. S. Bunting) Madison; Y. aig ag
X. plowmanii Bogner*: X. riparium E.
striatipes (Kunth) M Madison: X. UE
Rusby: ө SP nov. [ined.]*
Zomicar]

Z. о Mart. ex Schott

PROGRESS IN ORNAMENTAL
AROID BREEDING
RESEARCH!

R. J. Henny, D. J. Norman, and J. Chen?

ABSTRACT

Interest in development of new tropical ornamental aroid cultivars has accelerated ари) during the past 20 years.

This was stimulated by high market demand and newly published research that pres

sented potential breeders with

techniques to control aroid flowe "ring by application of gibbere llic acid sprays. In addition, research demonstrated how

seed production could be enhane ed by controlling relative humidity in aroid genera that

were previously difficult to

hybridize. Subsequent genetic studies showed foliar * patterns to be simply inherited, which made planning

crosses easier. This paper reviews some of the important tec
ey words: Anthuri
seed production, Spathiphyllum, 5

Aglaonema,

niques used in developing new ornamental aroid cultivars.

‚ Araceae, aroid, Dieffe nbachia, flowering, foliar variegation, plant breeding, seed,

Ornamental aroids are a major component of the

—

S. foliage plant industry and account for roughly
one-third of total ornamental foliage plant sales
(Fig. 1). The most important commercial ornamen-
tal aroid genera include Aglaonema, Anthurium,
Dieffenbachia, Epipremnum, Philodendron, Spathi-
phyllum, and Syngonium (Henny, 1988b). All are
valued for their showy foliage and ability to grow
under interior conditions of relatively low light and

relative humidity. The colorful and long-lasting
spathes of some Anthurium species are highly val-
ued as cut flowers, and the showy, white Spathi-
phyllum spathes enhance its popularity as a “flow-
ering” foliage plant. Syngonium and Epipremnum
are grown as hanging baskets or on totem poles.
The other genera discussed here produce inflores-
cences with no ornamental value; in fact, their in-
florescences are considered a nuisance by com-
mercial producers because they decay after
anthesis, remain unsightly, and must be removed
before sales. Many research papers have been pub-
lished regarding culture of ornamental aroids since
1970 (Conover & Poole, 1984; Joiner, 1981). Most
genera require shade and prefer high humidity and
warm temperatures. A basic rule of thumb is that
light intensities should be low enough to preclude
your hand from casting a shadow during the bright-
est part of the day. Light meter readings should be

1500-3500 foot Winter
should be 60°F minimum to prevent chilling injury

candles. temperatures
or 70°F to maintain growth. Soil mixes should drain
well and contain at least 50% organic matter by
volume. These are only general recommendations
for growing potted aroids, because some aroid gen-
era thrive in full sun, sandy soils, and do recover
from freezing.

Historically, new ornamental aroid cultivars orig-
inated either from mutations of established culti-
vars or from introduction of new plants collected in
the wild (Wilfret & Sheehan, 1981). During the past
20 years, however, plant breeding has had an ex-
panding role in the introduction of new cultivars.
Different aroid genera that are currently being bred
at the Mid-Florida Research and Education Cen-
ter—Apopka, including their important horticultural
traits and named hybrids released, are listed in Ta-
ble 1. Increased knowledge of aroid breeding meth-
ods and the development of plant tissue culture for
fast. reliable propagation have stimulated new aroid
cultivar development. Both of these factors were
fostered in part by their market’s high crop value
and its demand for new cultivars. Using tissue cul-
ture, a new aroid cultivar can be propagated rapidly
to commercial production levels within one to two
years instead of five to seven years required utiliz-
ing standard cutting or division techniques.

‘Successful breeding of new plants of any plant genus requires a source of diverse germplasm. We are fortunate that

many excellent botanical gardens and personal collections exist, and tha

t their plant materials have been generously

made available for our research purposes, We indeed owe much to many dedic 'ated botanists, horticulturists, and avid

plant people who work

tirelessly collecting and cataloging data on new

ources of aroids. Without their continued

efforts, the development of new ornamental aroid cultivars would be severe к limited. We extend a heartfelt thanks to

all of

them.

Florida Agricultural Experiment Station Journal Series No.

University of Florida, IFAS. |

32703, U.S.A. RJHennyOmail.ifas.ufl.edu.

ANN. Missourt Bor.

Mid-Florida Research and Education Center, 2725

10310.
Apopka, Florida

Binion Road,

GARD. 91: 464-472. 2004.

Volume 91, Number 3
2004

Henny et al.
Aroid Breeding Research

Figure |
(clockwise from bottom right), Anthurium, Dieffenbachia, Aglaonema. Spathiphyllum, and Aglaonema.

FLOWER STRUCTURE AND FLOWERING CYCLES

Aroid inflorescences consist of a spadix enclosed
by a spathe. The spadix is a fleshy spike covered
with many small unisexual or bisexual flowers, de-
pending on the genus. Aglaonema, Dieffenbachia,
Philodendron. and Syngonium display unisexual
flowers: they contain male flowers on the upper hall
and female flowers on the lower portion of the spa-
dix, with a small area between that may be devoid

flowers. Anthurium, Epipremnum, and Spathi-
phyllum have bisexual flowers. In these, the entire
spadix is covered with complete florets.

For breeding, flower production is vital. The ide-
al situation exists in mature Anthurium, where flow-
er production is continuous throughout the year for
many species. Differences in the natural flowering
cycles of some aroid species within the same genus
can be frustrating for plant breeders. Careful plan-
ning is required to ensure a sufficient supply of
flowers for breeding. especially in genera such as
Aglaonema and Dieffenbachia, which only produce
three to five inflorescences per ste Nat-
ural flowering of Aglaonema, Dieffenbachia, Philo-
dendron, and Spathiphyllum occurs in late winter

r spring 1 1 Florida (flow-

ering times vary depending on зое con-

m per year,

1 heated greenhouses

Different aroid hybrids used in the Mid-Florida Researe ‘+h and Education Center foliage breeding program

ditions. species, and cultivars). For example, in a
greenhouse heated to a minimum night temperature
of 50°F, plants of the same species or cultivar will
in a

flower approximately one month later than
comparable greenhouse heated to 60°F.
FLOWERING

CHEMICAL INDUCTION OF

At the Mid-Florida Research and Education
Center in Apopka, our aroid breeding program has
benefited from studies that revealed that Dieffen-
bachia 1980a). y Mp о (Henny.
1981). Syngonium (Henny et al.. 1999), and Agla-
onema (Henny 1983b) can be induced to flower
throughout the year if plants are treated with gib-
acid (СА), Treatment
generally consists of a
ppm GA, from a commercially available GA, source
(GibGro, 4% gibberellic acid, Agtrol Chemical
Products, Houston, 77074) and mixed at |
ounce per gallon of water. Following treatment,
plants will flower in three to five months, depending
on the genus. Fortunately, different species and
cultivars within a genus generally flower together
An additional benefit of

(Henny,

berellic a plant hormone.

single foliar spray of 250

Texas

following GA, treatment.
[e] 3

using GA, to induce flowering is that treated plants
produce more flowers than those not treated. Some

466

Annals of the
Missouri Botanical Garden

Figure 2.
the bud slage; day ol

Dieffenbac hia inflorescences (left to right) in
anthesis with spathe unfurled and
n for pollination; with ЫА n produced two days
fter anthesis; and with spathe partially removed to show
wd fe male iaa

inflorescences produced via GA, treatment may be
deformed, but no detrimental effects on fertility as
measured by pollen production or seed set have
been observed.

POLLINATION TECHNIQUES AND POLLEN
GERMINATION

Anthesis in Aglaonema and Dieffenbachia is in-
dicated by the unfurling of the upper spadix to ex-
pose the male flowers, a time when female flowers
are receptive (Fig. 2). However, pollen on the same
inflorescence is not dehisced until two days later
(Fig. 3). It is therefore necessary to obtain pollen
from another inflorescence and manually transfer it
to the seed parent. This can be done by brushing
pollen into a small container. If desired, the entire
inflorescence may be removed and situated so the
spathe catches pollen that becomes dislodged from
the spadix. Pollination can be easily accomplished
utilizing the brush employed to collect the pollen.
It is helpful to make the brush somewhat sticky by
touching the stigmatic surfaces of female flowers
before dipping it into the pollen supply for transfer
to the stigmatic surfaces of receptive flowers (Fig.

Figure 3. A
on a single Die И inflorescence showing pollen be-
ig dehisced

close-up (30X) of individual male flowers

Pollen germination studies with Aglaonema re-
vealed that although seed was obtained from flowers
that were pollinated one day after spathe unfurling.
the number of seeds was reduced (Henny, 1988a).
Receptivities of Aglaonema and Dieffenbachia flow-
ers last at least 24 hours. Female flowers’ stigmatic
surfaces do not support pollen germination once
pollen is produced by male flowers within the same
inflorescence (Henny, unpublished). By this time,
stigmatic surfaces have become discolored and soft.

Immediately following pollination, Dieffenbachia
flowers require 100% relative humidity to ensure
pollen germination (Henny, 1980b). This can be
done by wrapping the entire spadix with moistened
paper toweling within a plastic bag (Fig. 5). The
bag should be removed the next morning so it does
not interfere with pollen production. Maximum pol-
len germination (Fig. 6) and seed yield (Fig. 7) in
Aglaonema also requires high relative humidity af-
ter pollination (Henny, 1985).

n genera with bisexual flowers (e.g., Anthurium
and Spathiphyllum) the spathe unfurls and exposes
the spadix several days before female flowers are
receptive. Male and female Spathiphyllum flowers

Volume 91, Number 3 Henny et al. 467
4 Aroid Breeding Research

Figure 4. Pollination of a Dieffenbachia inflorescence using a soft brush.

Table 4
for in each genus, and a summary of the hybrid cultivars released by Mid-Florida Research and. Education. Center,

\popka. Florida.

V listing of the five aroid genera, major species used in breeding, important horticultural traits to select

Important species Important traits to Hybrid cultivars
Genus used in breeding select for in hybrids released by MREC
lelaonema nitidum (Jack) Kunth leaf shape and variegation pattern Stripe
commutatum Schott petiole color Flamingo
costatum М. E. branching and vigor Silver Bay
rotundum N. E. Br. chilling resistance Golden Bay
Anthurium andraeanum Linden early flowering Southern Blush
amnicola Dressler flower color and size Red Hot
antioquense Engl. branching and vigor Show Biz
crystallinum Linden & Andre disease resistance
scherzeranum Schott compact growth habit
Dieffenbachia imperialis Linden & Andre leaf "ie and color Triumph: Victory
leopoldii W. Bull petiole color Tropic Star: Sparkles
maculata D D. Don branching aa vigor Star White: Star Bright
stedtit Schott disease and chilling resistance Starry Nights
Spathiphyllum рен (Dryland) Schott early flowering none*
floribundum (Linden & Andre) continual эы ring
N. E. Br.
ard Савр N. disease resistance
wallisii Regil male sterility
Syngonium auritum (L.) Schott leaf color and size none**
podophyllum Schott branching
wendlandii Schott dwarf size

disease resistance

* Several hybrids released in 1998-1999 for propagation and trial growing.

New program initiated during 1999.

Annals of the
Missouri Botanical Garden

Figure 5.

A Die „ inflorescence wrapped in wet
eling and enclosed in a plastic bag for one day

paper tow
immediately after pollination to ensure pollen germination.

Anthur-
ium, female flowers at the base of the spadix mature

mature over a two- to three-day period. In

first and. gradually over a two-week period, addi-
tional florets become receptive toward the top of the
1968).
receptivity is indicated by a glistening shine of stig-

spadix (Kamemoto et al., In these genera,

matic surfaces.

Once no longer receptive, stigmatic surfaces dry
and turn brown. At this stage pollen appears along
the spadix's base, proceeding toward the top. Be-
cause of the uneven maturation of individual male
flowers, Anthurium pollen is available for up to two
weeks, while Spathiphyllum pollen can be harvest-
ed for two to three days. Anthurium pollen can be
transferred by collecting it on your finger tips then
gently rubbing it on receptive stigmas. Spathiphyl-
lum pollen is readily collected by gently tapping
the inflorescence and collecting the pollen as it
falls into a container held underneath. Subsequent
pollinations are made using a soft brush.

>

о achieve maximum seed production, an An-

thurium spadix may need to be pollinated more

than once because, as discussed above. female

flowers mature sequentially from the bottom to the

top of the spadix over a two-week period. However,
it is possible to fertilize an entire Spathiphyllum
spadix with one pollination if you wait until all the
styles appear receptive, which may require two to
three days. Following pollination, no environmental
manipulation regarding increasing relative humid-
ity, as is required with Aglaonema and Dieffen-
bachia, is needed to ensure Anthurium or Spathi-
phyllum seed set.

Very little information is available on aroid pol-
len storage. Pollen in short supply can be stored in
a container in a refrigerator and a high humidity
environment. Enclose the container with, but not in
contact with, a wet paper towel or some other moist-
Philodendron and Spathiphyllum
pollen may be stored

ened material.
in this manner for several
days to weeks. Aglaonema and Dieffenbachia pollen
germination declines within one to two days of stor-
age, so it is best to use fresh pollen for them.
SEED DEVELOPMENT AND GERMINATION
Dieffenbachia fruits mature in five to six months
(Fig. 8), Anthurium fruits require six months, and
Aglaonema fruits mature in four to six months, al-
though some hybrids have taken up to one year. In
Dieffenbachia and Aglaonema, seed maturity is in-
dicated by a Anthurium and
Spathiphyllum spadices begin to change color, soft-

red seed covering.

en, and seeds become visible.

To enhance germination, seeds are separated
from the spadix to lessen the chance of disease
contamination from the decaying fruit. For Dieffen-
bachia and Aglaonema, which have large seeds, the
fleshy seed covering is removed from picked, red,
berry-like fruit before planting the seed. Genera
with large numbers of small seeds such as Spathi-
phyllum are more difficult. The entire spadix is
placed in a plastic bag with a little water, The spa-
dix decays in a few days, allowing the seeds to be
removed by gently washing them on a screen small
enough to allow only the rotted spadix tissue
through. Cleaned seeds should be planted before
they dry.

High germination is achieved if seeds are sown
on top of a moist medium containing up to 50%
peat moss by volume and covered with plastic to
prevent drying. Aroid seeds begin to grow as soon
as sown. The medium should be kept at a minimum
of 70°F. Seedlings are repotted after the first true
leaves are produced. Most aroid seedlings require
one year of growth before they are evaluated.
INHERITANCE OF FOLIAR VARIEGATION

Foliar variegation in Dieffenbachia and Aglaone-
ma is dominant over non-variegation (i.e., green

Volume 91, Number 3 Henny et al.
2004 Aroid Breeding Research

Figure 6. A single Aglaonema flower pollinated at high (100%) re ‘lative humidity. Many pollen tubes are evident

on the stigmatic surface

оше 7. Several developing Aglaonema fruit at four months after pollination, Each fruit contains a single seed.

The тий turn re 4 when mature.

Annals of the
Missouri Botanical Garden

.

—

Figure 8. Three Dieffenbachia inflorescences with mature fruit that have been harvested for cleaning and planting.

Figure 9. Foliar variegation patterns (left to right) of Dieffenbachia maculata ‘Perfection, D. m. ‘Camille’ and a
hybrid containing the alleles for both patterns. The ‘Camille’ pattern masks the ‘Perfection’ pattern except near the
outer leaf edges.

Volume 91, Number 3
2004

Henny et al.
Aroid Breeding Research

Figure 10. Fo

iar variegation patterns (left to right) of

"Curtis, ane

‘Ernesto’s Favorite. A. л

\glaonema nitidum

their hybrid (right). which expresses a combination of both parental foliar variegation patterns.

leaves). A single dominant allele (Pv) determines
the presence of a variegation pattern typical for 4.

1982). Studies

showed that mutation of the Pv allele to Pv’ pro-

maculata “Perfection” (Henny,
duced the variegation pattern present in D. macu-
lata ‘Camille’ (Henny, 1986b). The Pv! allele masks
the expression of the Pv allele (Fig. 9). Inheritance
Dieffenbachia is also

controlled by a single dominant gene linked to the

of a white foliar midrib
gene controlling foliar variegation (Henny, 1983a).
The dominant alleles for each trait are carried on
opposite, homologous chromosomes.

Inheritance of foliar variegation in Aglaonema is
similar to Dieffenbachia. Six foliar variegation pat-
terns of Aglaonema have been reported to be gov-
erned by a single locus, multiple allelic system,
wherein each distinct pattern is controlled by a
1986a). АП six

alleles studied were codominant: therefore. a max-

separate dominant allele (Henny,

imum of two variegation patterns in the same plant
could be expressed (Fig. 10). Plants that were het-
erozygous for variegation would express only one
pattern while homozygous recessive plants would
be nonvariegated. The combination of two different
variegation patterns in a single hybrid has allowed
creation of plants with novel patterns (Henny,

1986a). Additional variegation patterns in Aglaone-
ma are currently being studied and appear to be

inherited in the same manner.

Literature Cited

& К. T. Poole. 1984. Light and fertilizer rec-

ommnie ad for po tion of ace лапы d p d foli ige

—

jonovt

plants. AREC-A Research Report t RH-84—7 рр:
Henny, R. J. 1980a. Gibbere lic acid (G ^ ) эы. es flow-
ering of Dieffenbachia maculata ‘Perfection’ Hort-

5: 613
19% 30b. Re lative humidity affects in vivo pollen
pre eis zn in м л та-

Science 15

germination and seec

culata “Perfection.” J. Amer „ Hort. . 105: 546-
5

. 1981. Promotion of flowering in iir da
‘Mauna Loa’ with gibberellic acid. HortScience
5541-5595.

—. 1982. Inheritance of foliar v

Dieffe 1 cultivars. J. Heredity 73: :
‚ Inheritance of the white iie midrib in
Dieffe ae and its linkage with the foliar variegation.

J. Heredity 74: 483-484.

1983b. Aglaonema commutatum
"Ireubir epa treatment with gibberellic acid.
HortScience 18: :
1985. In vivo ‘pollen germination of Aglaonema
affec ted 55 1 humidity. HortScience 20: 142—143.
1986a. Single locus, multiallelic inheritance of

variegation in two

Е ae ring of

Annals of the
Missouri Botanical Garden

foliar variegation in Aglaonema. J. Heredity 77: 214—
215.
1986b. Inheritance of foliar variegation in Hi A
Жы "hia maculata “Camille. J. Heredity 77: 285-286
. 1988a. Pollen ge nen in, . ma flowers
of die re «el ages. HortScience : 216
— ———. 1988b. Ornamental мн
Рр. ee in J. Janick
Vol. X.

1

and breeding.
Horticultural Reviews

(editor),
1 r Press, Portland, Oregon.
). J. Norman & M. E. Kane. 1999, Gibberellic

ac 'id-induced flowe ring of ундоп. p
Schott ‘White dur rfly’ HortScience 676-67

Joiner J. N. 198 5 Plant Piodnolion. ranile e-

, Engle er c liffs, New Jersey.

fia moto „II., Н. 1 sone & M. Aragaki. 1968. Im-
proveme nt of nd through E Proc. Tro
Region ai IT . Hort. Sci. 5727.

W ilfret, G. J. & T. J. ‘Shee shan. 1981. Pere Ж nt of new
oe ун М can Pp. 36. in J. Joiner (edi-
tor), Foliage Plant Pion Prentice-Hall, Engle-

wood c Lita. New Jers

س

A PRELIMINARY SURVEY OF Eduardo G. Gonçalves,” Élder A. 5.
PETIOLAR COLLENCHYMA Paiva,” and Marcus A. Nadruz Coelho!
IN THE ARACEAE!

ABSTRACT

species from 56 genera po ly 51% of the

This article presents а preliminary systematic survey of 115
and classified. This feature

genera) of Araceae in which the pattern of petiolar мере hyma (or its absence) is describe
rently not changing qualitatively with development: " or environmental

appears very conservative within the genera, appa
studied, but apical and basal

р
conditions. Cross sections at the midpoint between petiole base and apex were mainly s
sections were also observed in those genera where the collenchyma is absent at petiole midpoint. Three patterns are
defined: (1) collenchyma absent at ilo midpoint between petiole base and apex; (2) a peripheral continuous or inter-
ed ring of collenchyma (philodendroid pattern): (3) rounde р strands of collenchyma concentrically disposed апа
ds genera with bisexual flowers so far analyzed have
vase. Monoecious genera сап display all

ase

rupte
associated with periphera il vascular bundles (colocasioid pattern
collenchyma at petiole midpoints, although this usually occurs at apex and |
three patterns, but pattern 1 appears restricted to tribe Zamiocule ا‎ and the genus Anubias. The presence of a fully
collenchymatous petiole seems to appear only in more derived genera in the Araceae: it may be an apomorphic feature
within ihe amily.

Key words: Araceae, collenc 'hyma, petiole, pulvinus, sclerenchyma.

and he published most of the current. knowledge

Anatomical features are, in many Cases, reason-
about this topic. Engler considered the patterns of

ably important for the taxonomic definition of some
groups and are considered to be as valuable as mor- collenchyma taxonomically meaningless because
phological ones (Stace, 1980). In taxa in which gross they were not congruent with his classification. Lat-
er Solereder and Meyer (1928) described the peti-
of comparative plant anatomy are very useful. ole anatomy in various species, observing a fused

The anatomy of the Araceae has been studied ring of collenchyma in Asterostigma, Dieffenbachia,
mainly by French (1997). His studies have been Homalomena, Philodendron, Schismatoglottis, and
Spathantheum. They also observed that Peltandra,

morphological features are. non-informative, studies

important in helping to define the supra-generic
classification of the family (Mayo et al., 1997). De- Typhonodorum, many genera of the tribes Caladieae
and Colocasiae, and most Old World Areae had col-

spite the broad range of these studies (across taxa
lenchymatous sheaths associated with the vascular

and across organs and tissues), little attention has
been directed to leaves and petioles. bundles.

Although restricted in its occurrence. in the In a short communication on the determination
monocotyledons (Fahn, 1990), collenchyma is of collenchyma patterns in the Araceae, Gongalves
and Paiva (1995) described two basic patterns of
distribution of this tissue in petioles. They were
and “philodendroid,” based

—

found in various genera of the Araceae. It is com-
mon in growing aerial organs as supporting Ussue,
being characterized by the presence of thick-walled named *colocasioid"
on the Englerian subfamilies in which each pattern
was first observed. The former was characterized by
the presence of rounded strands of collenchyma
concentrically disposed and the latter by a ring of
collenchyma surrounding the whole petiole that
could be either continuous or interrupted.

cells with non-lignified 5 walls. Collenchyma
is also noted for its plasticity, i.e., this tissue retains
its capacity to be deformed, 1 its function

is related to mechanical support.
Probably the first to observe patterns of support
tissue in petioles of Araceae was Engler (1920),

! We thank those that contributed by sending living plants or seeds to be surveyed, We are also grateful to Richard
Keating for important sugge gx and Simon Mayo for the revision of an earlier version of the manuscript. Part of this
work was conducted at the University of Brasília. DF, Brazil. During the course of this work, EGG was funded by
grants CAPES and F AP ESP aze
? Universidade Católica de Brasilia, Curso de Ciências Biológicas, Prédio Sào Gaspar Bertoni, sala M-206, QS 7
Lote 1, EPTC, CEP 72030-1 55 Paid DF, Brazil.

sae an de Botánica. Universidade Federal de Minas Gerais. Caixa Postal 486—CEP 31270-901, Belo Horizonte,
MG, Brazil.

Jardim Botánico do Rio de Janeiro, Rua Pacheco Leáo 915, CEP 22460-030, Rio de Janeiro, RJ, Brazil.

ANN. Missourt Bor. GARD. 91: 473-484. 2004.

474

Annals of the
Missouri Botanical Garden

Given the potential significance of such a feature
for phylogenetic studies in aroids, we present here
a preliminary survey of petiolar patterns of collen-
chyma in the Araceae.

MATERIALS AND METHODS

Plants from 56 genera were surveyed, covering
approximately 51% of the currently accepted gen-
era for the family (109), This number of genera in
the family was calculated using the previously ac-
1997) minus
Lazarum (Hay, 1997) minus Sauromatum (Hetter-
scheid & Boyce, 2000) (both merged with Typhon-
tum) plus the five genera of “lemnoids” (French et
al., 1995; Les & Crawford, 1999). We analyzed 115
species (Table 1), all from fresh material. When

cepted number of 106 (Mayo et al.,

possible, more than one species for each genus was
sampled in order to observe the infrageneric vari-
Wild-collected

plants or aroids of cultivated origin were used

ation. of collenchyma patterns.

(vouchers are deposited in the herbarium of the
University of Brasília). Since many non-Brazilian
genera were sampled from cultivated material (usu-

ally from unknown origin), we also vouchered all of

them. All plants were identified and surveyed for
the pattern of supporting tissues in the petioles.

To determine the pattern of collenchyma, fully
expanded foliage leaves were collected. Transverse
sections at the midpoint between petiole base and
apex were studied, except in Pistia stratiotes, in
which the base of the sessile leaf was used. Mate-
rial not collected near the laboratory (e.g.. from
wild populations) was preserved in 50% glycerin
solution to keep it hydrated and preserve the col-
lenchyma. In some genera with bisexual flowers,
sections were also made at the base and/or apex of
the petiole, particularly when a pulvinus was pre-
sent.

Transverse sections were made by hand from
each petiole. The sections obtained were submitted
to a vacuum to remove air bubbles from the tissue.
The sections were then stained using Astra Blue
and Fuchsin counter stains or subjected to histo-
chemical tests for pectins (Ruthenium Red) and lig-
nins (acid phloroglucin) (Johansen, 1940). The sec-
tions were then mounted in semi-permanent
preparations with aqueous glycerin.

The collenchyma patterns were recorded by light
photomicrography and drawn using a drawing at-
tachment model Olympus BH2. A complete list
with all material surveyed is presented in Table 1.

RESULTS

For our preliminary observations, it was noted
that the pattern of distribution of collenchyma in

the petioles of the Araceae does not change qual-
itatively with the age of the plants. As far as our
analysis showed, all species from the same genus
presented the same patterning, which suggested
that variation in the pattern of collenchyma be-
It was
also observed that there was no significant change

tween taxa could be taxonomically useful.

in relation to growing conditions.

The collenchyma patterns observed of all sur-
veyed taxa are shown in Table 1. Three patterns
were identified (see Fig. 1): (1) collenchyma absent,
at least from the midpoint of the petiole (Fig. 2A)
presenting sclerenchyma as the main supporting
tissue; (2) a peripheral ring of collenchyma (phil-
odendroid pattern) (Fig. 2C), which can be either
continuous or interrupted; (3) rounded strands of
collenchyma concentrically disposed. (colocasioid
pattern) (Fig. 2D). All taxa studied could be re-
ferred to one of these patterns, as follows:

SUBFAMILY POTHOIDEAE

The representative genus considered was An-
thurium with the nine observed species showing no
collenchyma at the midpoint between petiole base
and apex. The vascular bundles are accompanied
by sclerenchyma and some species (e.g., А. acutum
and А, longifolium) have the outermost vascular
bundles united by a continuous sheath of scleren-
chyma.

SUBFAMILY MONSTEROIDEAE

The taxa studied here include Heteropsis (1 spe-

—
—

cies), Rhaphidophora (1), Epipremnum (1), Scin-
dapsus (1), Spathiphyllum (5), Stenospermation (2),
Monstera (2), and Rhodospatha (2). All surveyed
genera lacked collenchyma at the midpoint be-
tween petiole base and apex.

SUBFAMILY LASIOIDEAE

The genera surveyed were Cyrtosperma (1 spe-
cies), Dracontium (2), Dracontioides (1), Lasia (1).
Pycnospatha (1), and Urospatha (1). None of the
genera have collenchyma at the midpoint between
petiole base and apex.

SUBFAMILY AROIDEAE

With the exception of Zamioculcas, Gonatopus,
Anubias, and Ambrosina, where collenchyma is ab-
sent from petiole mid regions, all genera from this
subfamily present true collenchyma as the main
supportive tissue in the petioles. The collenchyma
may be isolated from the epidermis by a few layers
of parenchyma (e.g., Aglaonema crispum and Dief-

475

Volume 91, Number 3

2004

Gongalves et al.

Petiolar Collenchyma in Araceae

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Petiolar Collenchyma in Araceae

Gongalves et al.

Volume 91, Number 3

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Petiolar Collenchyma in Araceae

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Volume 91, Number 3 Goncalves et al.
2004 Petiolar Collenchyma in Araceae

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Annals of the

482

Missouri Botanical Garden

Volume 91, Number 3
2004

Gongalves et al. 483

Petiolar Collenchyma in Araceae

fenbachia paludicola), or may be in direct contact
with the epidermal cells (e.g., Mangonia tweeedi-
ana, Homalomena wendlandii, and Asterostigma
riedelianum). The thickness of the collenchyma (as
well as the number of cell layers on it) is a variable
feature among genera and also among species from
the same genus. In Dieffenbachia paludicola, the
thickness of the collenchyma ring ranges from 4 to
10 cell layers, and appeared to be thicker in bigger
leaves.

In the genera Dieffenbachia (3 species), Philo-
dendron (11), Homalomena (2), Aglaonema (4), and
Zantedeschia (3), and all surveyed genera from the
tribes Spathicarpeae (8 genera, 13 species),
Nephthytideae (2, 2), and Montrichardieae (1. 1),
as well as in the genus Schismatoglottis (2). the
collenchyma forms a cortical ring (philodendroid
pattern), which can be continuous (as in Mangonia
and Asteros-

tweedieana, Taccarum weddellianum,

tigma cryptostylum) or segmented by intrusions of

parenchyma. These intrusions may be narrow (1 to
4 cell layers) as occur in Dieffenbachia elegans and
some Philodendron species (e. g., P. uliginosum and
P. pedatum) or wider, as observed in Aglaonema
modestum (up to 8 cell layers). The Asian genus
Aglaonema deserves special mention. In three of
the four sampled species of Aglaonema (A. com-
mutatum, A. modestum, and A. costatum) the cor-
tical ring of collenchyma is so widely interrupted
that the segments can be classified as strands.
However, since they are not associated with vas-
cular bundles, we prefer to assign this genus as
having a philodendroid pattern. In any case, Agla-
onema crispum has a “typical” philodendroid pat-
tern, showing a segmented cortical ring of collen-
chyma.

It was observed that the position of the paren-
chyma intrusions usually coincides with the occur-
rence of stomata in the epidermis in all species in
which they occur. Such an aspect needs further in-
vestigation in order to verify how permeable to air
diffusion is the collenchyma.

In genera with rounded strands of collenchyma
(colocasioid pattern) as in all surveyed Areae (2
genera, 7 species), Peltandreae (2, 2), Caladieae (4.
14), Colocasieae (2, 4), Arisaemateae (2, 2). Cryp-
tocoryneae (1, 1), and Zomicarpeae (1, 1), each col-
lenchyma strand is associated with vascular tissues.

Such strong association (31 sectioned taxa) may
suggest that the vascular bundles share in the on-
togenesis of their associated collenchyma strand.
In those genera of subfamily Aroideae in which
the collenchyma is absent at the mid regions of the
petiole, two different conditions were observed. In
Zamioculcas, Gonatopus, and Anubias, there is
sclerenchyma associated with the vascular bundles
as in all surveyed genera with bisexual flowers (e.g..
Anthurium, Monstera, etc.). In Ambrosina no sup-
porting tissue, collenchyma or otherwise, could be

observed in the petioles.

DISCUSSION

Based on the patterns of collenchyma. our stud-
ies do not support the distinction of subfamilies

Colocasioideae, Aroideae, and Philodendroideae,

as formulated by Engler and Krause (1920) and

—

ater by Grayum (1990) as well as Bogner and Nic-
olson (1991). This conclusion was reached previ-
ously by Mayo et al. (1997) using cladistic analysis
of morphological and anatomical characters, as well
as by French et al. (1995) using analysis of restric-
tion fragments of chloroplast DNA. The subfamily
Aroideae (in its broad sense) can here be circum-
scribed as including plants with a fully collenchy-
matous petiole, in a philodendroid or colocasioid
pattern. Exceptions are the small tribe Zamiocul-
cadeae (both Gonatopus and Zamioculcas), Anubias
and Ambrosina (Ambrosineae), i

—

(Anubiadeae),
which the absence of collenchyma is here stated as
secondary.

Distribution of the colocasioid and philodendroid
patterns within the Aroideae seems to support the
two major clades proposed by French et al. (1995).
All genera herein belonging to French’s clade with
Grayum’s Philodendroideae minus Peltandra alli-
ance plus Zamioculcadeae plus Stylochaeton have
a philodendroid pattern of petiolar collenchyma.
The only exceptions are the African tribe Zami-
oculcadeae and the African genus Anubias. The
surveyed genera from French’s clade with Grayum's
Aroideae plus Peltandra alliance plus Colocasioi-
deae have a colocasioid pattern of petiolar collen-
chyma. The exceptions are Ambrosina, in which the
collenchyma seems to be absent, and Schismato-
glottis, in which the collenchyma is clearly philo-

¢

Figure 2. ‘Trans
apex. —B. Pulvinar region. Philodendron cipoense:—
tatum:—D. Midpoint, between petiole

vascular bundle, co = collenc ا‎ .)

sversal sections of the petioles. о за pinnatum:—A. Midpoint, between petiole base and
idpe
base and apex. (Scale bare = 100

point, between petiole base and a apex. 1 ا‎ angus-
epidermis, fb = fibers, vb =

pm: ep =

Annals of th
Missouri Bod Garden

dendroid. Interestingly, the tribe Schismatoglotti-
deae (five genera, only Schismatoglottis here
surveyed) comprises the most basal clade within
the huge Aroideae plus Peltandra alliance plus
Colocasieae clade published by French et al.
(1995), together with the clade Cryptocoryne plus
Lagenandra.

In contrast, the African genera Gonatopus and Za-
mioculcas (tribe Zamioculcadeae) do not have col-
lenchyma in the petioles, and sclerenchyma com-
prises the main supporting tissue (although the
collenchyma can occur in the apex and base of pet-
ioles or in the median pulvinus of Gonatopus). Both
Old World genera Gonatopus and Zamioculcas were
earlier placed in subfamily Pothoideae (Engler,
1905), but were later excluded and added to La-
sioideae by Bogner and Nicolson (1991). Mayo et al.
(1997) moved both genera to the huge subfamily
Aroideae, accommodating them in tribe Zamiocul-
cadeae. Moreover, both genera possibly branched
early in the evolutionary history of the Aroideae
(Mayo et al., 1997). An alternative hypothesis con-
cerns their habitat. Both genera occur in southeast-
ern Africa and are subjected to strongly seasonal
rainfall. A secondary loss of the collenchyma to in-
crease drought resistance is one possible explanation
for Well-developed sclerenchyma is
thought to reduce the injurious effect of wilting in
the leaves of xerophytic plants (Esau, 1977).

its absence.

Another African genus in which collenchyma is
restricted to the apical pulvinus is Anubias. We sur-
veyed two species (A. afzelii and A. hastifolia), and
both have sclerenchyma as the main supporting tis-
sue. Since Anubias is not considered a basal taxon
within the philodendroid clade (see French et al.,
1995), we consider that the fully collenchymatous
petioles were secondarily lost.

The absence of collenchyma in Ambrosina can
also be explained as a secondary loss. The mono-
typic genus Ambrosina comprises diminutive plants
(Mayo et al., 1997),
may make the presence of supporting tissues in the
petioles less adaptively significant. Further, most of
the length of the petiole remains under the soil.

In some genera with bisexual flowers (and also in
Zamioculcas, Gonatopus, and Anubias) some collen-
chyma may occur at the base and at the apex of
petioles (Fig. 2B). This occurs mainly when a pul-
vinus is present (French, 1997). This collenchyma-
tous portion at the apices and bases can be found

and their very reduced size

even when there is no morphologically distinct pul-
vinus. Such areas allow some plasticity to fully de-
veloped leaves. It is possible that the fully collen-

chymatous petiole of the monoecious genera arose

Масе, C. A. 1980. Pl:

in consequence of an increased development of the
pulvinus. It is note worthy that in the transition zone
between petiole-leaf blade, the sclerenchyma is al-
ways absent (or dramatically reduced), whether or
not the collenchyma is present. In some genera (e.g.,
Zamioculcas, Epipremnum) there is also a basal pul-
vinus that can be morphologically distinct or not. In
this case, the anatomical structure at the base is
similar to that of the apical pulvinus.

The monoecious genera have been considered to
be phylogenetically more derived than the genera with
bisexual flowers (French et al., 1995; Mayo et al.,
1997). Since the presence of a fully collenchymatous
petiole seems to coincidentally appear only in more
derived. genera of Araceae, its occurrence. probably
represents an apomorphic feature in this family.

Literature. Cited
Бейрек » &
tion

3 5—50.

2 г, А. 1 Araceae—Pothoideae. In A. Engler (edi-

tor), Das Obi: ‘ich 21V. 23B): 1-330.
1920. A Pars
ad

. Nicolson. 1991. A revised classifica
f Araceae n dichotomous kevs. Willdenowia 21:

eneralis et index familiae
(e i

raceae.
— In: A.
74(IV. 23А): 1—

K

Das Pflanzenreich.

—— & K. Krause. ‚ 1920. Araceae—Colocasioideae. In А
Engler re Das Pflanzenreich 71(IV. 23E): 1-139

Esau, К. 1977. Anatomy of Seed Plants, 2nd ed. John
Wiley & Sons, New York.

"ahn, A. 1990. Plant Anatomy, 4th ed. Pergamon Press,

Gambridge:

French, J. C. . Vegetative anatomy. Pp. 9-24 in S
Mayo, J. ые & P. C. Boyce da The Genera m
Araceae. я Botanic Gardens

— Chung & Y. K. Jur. 1005. C hloroplast DNA
phogen ny Ariflorae. Pp. 255-275 in P. J. Rudall,

J. Cribb, » Cutler & C. J. Humphries (editors),
M E ‘Syste matics and Evolution. Royal Bo-
tanic Gardens, Kew.

Gongalves, E. G. € E. A.

S. Paiva. 1995. Determinação
dos padróes de distribuicáo do colénquima no pecíolo
de algumas Araceae. Cuiabá: ie СП do Ш Encontro
de Botánicos a = entro Or 37.

Grayum, е e 19 d ue om of the Ar-
aceae. A rie Bot. ard. 20-697.

Hay, A. 1 997. Two new species Adi a new combination in
Australian eed e eae tribe Areae). Edinburgh

. Bot. 54(3 329- 336.

Hette rscheid,

fication

ste

‚ Boyce. ind A reclassi-

of асо 5 rm and a new species of

Typhonium Schott н ipa 'eae). ied fa 23: 48-55

Johanse s А А 940. Plant Microtechnique. 17 8
Hill, „ York.

Les. e . & D. J. Crawford. 1999, m ai mna-
ceae * a new genus of duc 5 Novon 9:

Mayo, S. J., J. Bogner & Р. С. . 1997,
of Arac ‘ru Royal aaa a] ew.

е, F. J. мун 1928. tematico he Anato-

ue der Mon А tyledon Heft 3. ا‎ -Synan-

ac Spire ;ebrüder ` Borni träger, Ber

ant Taxonomy and Трн ТРЕТЯ
Yor

)-533.
T i Genera

Edward Arnold, 1

VEGETATIVE ANATOMICAL
DATA AND ITS
RELATIONSHIP TO A
REVISED CLASSIFICATION
OF THE GENERA OF
ARACEAE!

Richard C. Keating?

ABSTRACT

Among structural data

ent compilation of anatomical literature and original anatomical investigations of the leaf and petiole of Araceae
the

1051 concis

2

as
led to a search for
sets summarized, useful pum 'rvations ine ‘luded those o
chyma, raphide crystals, and laticifers. These

systematic organization of the genera within this family.

YF type and position of conducting and mechanic val tissue, aeren-
data were superimposed on three lines of evidence using DNA sequences.

The revised classification resented | jen re e d in fewer anomalous generic placements and provides a framework

for pe rstanding the evolution of the family. Curre
and 2
Pos words:

anatomy, Araceae, DNA sequence,

Lemnaceae,

mtly 106 genera are recognized and divided among 9 subfamilies
tribes. The new subfamily Se эы кога ae is described

Se hismatoglattideidene taxonomy.

Our current image of the family Araceae was es-
tablished by Schott (1860), who assembled the gen-
era that we now call aroids. His classification was
based mostly on reproductive characters (see Gra-
yum, 1990, for a thorough review). Generic classi-
fication of the Araceae was refined during the 19th
and early 20th centuries by Engler, whose last ar-
rangement (Engler, 1920) was based on decades of
accumulated data. The standard he set was ahead
of its time in being based on a broad and inclusive
array of combined morphological and anatomical
observations, both reproductive and vegetative. His
keys and descriptions utilized habit, leaf arrange-
ment and shape, leaf venation patterns in consid-
erable detail, type of laticifers and relationship to
veins, mechanical tissue including distribution of
trichosclereids, inflorescence characters, floral
parts, their shapes and fusions, ovary locules, and
ovule position. His classification stood for about 50
years, and students of the family have traditionally
followed this broad “Englerian” approach to clas-
sification issues (cf. Grayum, 1990).

Also in this category is a classification for Japan
and adjacent areas by Hotta (1970), whose Engler-
ian approach was later documented in detail (Hotta,
1971). Bogners (1979) presentation of Engler's
classification updated the changed generic con-
cepts occurring in intervening time. Similarly, Bog-
ner and Nicolson (1991) continued this work, re-

moving Acorus from the family (see Grayum, 1987),
and producing useful keys that invoked a wide va-
riety of reproductive and vegetative characters. A
half dozen additional rearrangements in tribal po-
sitions were proposed. Incrementally, Englers in-
frastructure was evolving.

Hutchinson’s (1973) arrangement emphasized
mostly reproduc tive characters in the spirit of
Schott and Hooker. His suprageneric infrastructure
subdivided the family into 18 tribes, an approach
not recognized by modern workers.

Comparisons of several classifications since En-
gler (1920) have been published by Nicolson
1988). Croat (1990), Mayo et al. (1997). and Keat-
ing (2002). These comparisons contrasted varying
concepts of aroid generic infrastructure and will not
Most frequently. groupings of

—

be repeated here.
genera into tribes or adjacent tribes are less con-
troversial, but there remain substantial differences
in recognition of subfamilies, their generic scope.
and their relative position. Subfamily relationships
are especially important to understand as they rep-
resent the base of evolutionary branches within the
family and point to the character of its early diver-
gence. Determining these relationships using struc-
tural characters is hampered by lack of understand-
ing of all instances of parallel evolution and
character reversals. For instance, Hotta (1971) not-
ed that tuberous growth, the climbing habit, and

' My thanks to Thomas Croat, Mike Grayum, Dan Nic end e an anonymous reviewer for useful critique, and also

“e on nomenclature and a Latin dia
Box 299, St.

to Roy Gereau for advic
2 Missouri Botanical Garden, P.O.

ANN. Missouni Bor.

Louis, Missouri 63166-0299, U.S.A. richard.keating(?mobot.org.

GARD. 91: 485—494. 2004.

486

Annals of the
Missouri Botanical Garden

compound leaf formation have arisen independently
among the several subfamilies.

In the 1980s, a number of anatomical contribu-
tions based on large generic samples were pub-
lished by French and collaborators (French, 1985a,
b, 1986a, b. c, 1987a, b, e, 1988; French € Tom-
linson, 1980, 198la, b, c, d, 1983, 1984;
view by French, 1997). These yielded a wealth of
comparative data requiring integration into an up-

see re-

dated view of generic evolutionary relationships.
Grayum (1990) provided a thorough review of use-
ful characters and proposed a revised classification.
which he claimed returns somewhat to pre-Engler-
ian concepts; that is, he makes the point that ge-
netic isolation begins with modification of repro-
ductive organs, and that we should be paying more
attention to these structures and to pollination sys-
tems. Still, he was comprehensive in his approach
to data analysis.

A compilation of vegetative anatomical data, in-
cluding original observations, has been assembled
by Keating (2000, 2002, 2003, 2004). These stud-
ies had three goals: understanding the limits of var-
iation of histological complexity, assessing the po-
tential of such data in understanding evolutionary
trends of specialization, and assessing their poten-
tial to be useful in delineating generic and supra-
generic categories.

As the project progressed, there arose the need
to choose a classification against which to arrange
the growing files of observations. The anatomical
trends. compared. against. classifications produced
up to 1995 yielded a number of anomalies that
made the choice difficult. Originally I had hoped
to use the classification of Mayo et al. (1997), but
their decision not to recognize several formal cat-
egories pending ongoing studies provided insuffi-
cient hypotheses for testing the relationship of an-
atomical data to a full classification. For example,
their large subfamily Aroideae, containing 74 gen-
era, included a group of 27 genera that are scat-
i tribal
those genera are placed in the

tered among “alliance” and “no alliance”
groupings.
subfamily Philodendroideae based primarily on
possession of banded or banded-interrupted (types
B, Bi, or Sb) collenchyma (see Keating, 2000, table

While this decision was pending, French et al.
(1995) published an analysis of cpDNA restriction
site data that included a sample of 85 currently
accepted genera. Their resulting consensus tree re-
inforced a number of traditional concepts regarding
the scope and recognition of subfamilies and tribes,
while also promoting new ways of conceiving of
some relationships. It became the obvious candi-

date against which to order the anatomical data.
The above-mentioned ordering of the 27 philoden-
droid genera exactly corresponded with the cpDNA
topology.

After the present contribution had been drafted,
| received consensus and bootstrap trees for the
family from Cabrera et al. (2003). They have com-
pleted sequencing two genes, rbcd and matK, for
94 taxa, and which included 3335 molecular char-
acters. Their topology resulted in a few generic
shifts in position from the French et al. (1995) re-
sults, which will be discussed in the context of sub-
families and tribes below. At final editing, 1 re-
ceived a copy of the work by Rothwell et al. (2004)
based on sequence data of the chloroplast trnL-trnF
intergeneric spacer. Thirty-six species of Araceae
and Lemnaceae were sampled for a study that dealt
especially with the relative positions of Lemnaceae
and Pistia.

After reviewing all contemporary classifications,
the approach toward developing this revision in-
volved (1) comparing anatomical data sets against
DNA sequence data; (2) inserting in correct se-
quence various genera that had not been sampled
[their placement was not controversial when re-
viewing Mayo et al. (1997) and other classifica-
tions]; (3) determining the level of recognition of
generic groupings; and (4) checking anatomical,
morphological, and geographic data for anomalies
or evidence of unparsimonious suprageneric con-
cepts.

The resulting classification (Appendix 1) appears
to reduce the need for unnecessary ad hoc hypoth-
eses of evolutionary relationships. French et al.
(1995) did not revise the classification of the family
after presenting their cpDNA tree. Also, some of
their more interesting conclusions were not adopted
in the new classification by Mayo et al. (1997), al-
though, to some degree, it influenced their generic
sequence,

Nomenclatural sources for family infrastructure
taxa in Appendix 1 include Kubitzki (1998), Lan-
dolt (1998), Mayo et al. (1997), Nicolson (1984),
and J. L. nomenclatural database
<www.inform.umd.edu/pbio/fam>). The genera
(marked *) not sampled by French et al. (1995)
were inserted in Appendix 1 following the recent

Reveal’s

—

classifications cited above and after checking the
evidence for anomalous anatomy.
COMMENTS ON FAMILY INFRASTRUCTURE

Some of the anatomical characters summarized
in the following systematic discussion are coded

Volume 91, Number 3
2004

Keating
Vegetative Anatomical Data

є

using typology that is defined in Appendix 2
in detail in Keating (2002).
The first five subfamilies contain genera pos-

and

sessing bisexual flowers.

SUBFAMILY GYMNOSTACHYDOIDEAE

This subfamily contains the eastern Australian
genus Gymnostachys, whose isolated taxonomic po-
sition is easily justified. Vascular bundles are
unique, having fibers that ensheath the bundles
with unusual cap and girder architecture. Collen-
chyma is absent.

The molecular genetic evidence indicates that
the genus clusters on the same branch with the
genera of Orontioideae, although structural data
suggest no such position. Its vasculature and un-
differentiated mesophyll structure resemble that of
no other aroids. With the removal of Acorus from
the family, Gymnostachys is the only remaining ge-
nus with linear leaves and parallel-organized sto-
mata. This and other unusual anatomy, especially
the unique form of leaf vascular bundles would for-
merly have suggested its separation from the family.

SUBFAMILY ORONTIOIDEAE

This subfamily is divided into two tribes. The
tribe Orontieae, containing only the eastern North
American genus Orontium, has acrodromous leaf
venation, phloem fiber collenchyma absent,

laticifers non-anastomosing, and raphide cells

caps,

bearing multiple crystal bundles.

Tribe Symplocarpeae, containing Lysichiton of
western North America, eastern Asia, and Japan.
and Symplocarpus of eastern North America, east-
ern Asia, and Japan, has leaves with pinnate ve-
nation, fibers absent, collenchyma types С and В,
and laticifers absent.

Molecular genetic evidence affirms the single
subfamily concept with Orontium being less closely
related to the other two genera. On this basis, and
on account of structural data, tribal-level recogni-
tion is warranted to reflect this distinction. Mayo et
al. (1997)

do not recognize tribes in this subfamily.

SUBFAMILY POTHOIDEAE

The 16 genera included here occur in the tropics
of Asia, Malaysia, Madagascar, and the Americas,
and Africa in the case of Rhaphidophora.

Tribe Pothoeae, containing Pothos, Pedicellarum,
Pothoidium, and Anthurium, has leaves and peti-
oles with type I vascular bundles; fibers ensheath-
ing vascular bundles: collenchyma absent; and la-
are encountered

ticifers absent. Trichosclereids

only rarely in Pothos.

Tribe Monstereae includes the 12 genera Hol-
ochlamys, Spathiphyllum, Rhodospatha, Stenosper-
mation, Scindapsus, Rhaphidophora, Anadendrum,

Monstera, Alloschemone, Epipremnum, Amydrium,

and Heteropsis. Anatomically, these genera share
types Гапа П vascular bundles: fibers ensheathing
vascular bundles or occurring as bundle caps: tri-
chosclereids in 9 of the 11 genera: collenchyma
type B or absent.

Grayum (1990) proposed this subfamily concept
but others have divided the genera among the Po-
thoideae and an adjacent subfamily Monsteroideae
(Mayo et al., 1997; Bogner & Nicolson, 1991). The
latter authors noted a lack of clear character dis-
tinctions supporting two subfamilies and also sug-
gested that the genera could be united.

On the basis of all structural and molecular ge-
netic evidence, no basis can be discerned to justify
subfamily-level distinction for the two included
tribes. For tribal separation, presence versus ab-
sence of collenchyma stands out as well as more
leaf variation in the Monstereae. The trichoscler-
eid-bearing genera have a strong tendency be
grouped in the Monstereae. That line of evidence
is weakened by the rare presence of trichosclereids
found in the petiole of one Pothos species and the
fact that two genera of tribe Monstereae, Amydrium
and Heteropsis, have none. In summary, even tribal
diagnostic differences are indicative but not strong.
SUBFAMILY LASIOIDEAE

The 10 included genera occur in the American
and Asian tropics, the Malay archipelago, and Af-
rica in the case of Lasimorpha. The genera are:
Cyrtosperma, Lasimorpha, Podolasia, Lasia,
phyllum, Urospatha, Anaphyllopsis. Pycnospatha,
Dracontium, and Dracontioides. Vascular bundles
are types Тапа IL fibers ensheath bundles or occur

Ana-

as bundle caps, collenchyma is type B or absent,
and the petiole usually develops type 4 air cavities,
an uncommon type within the Araceae.

Further tribal infrastructure in this subfamily is
unnecessary, as the morphology and anatomy of the
genera are distinct and uniform; in fact, as defined
here, the subfamily constitutes one of the more uni-
form groupings in the Araceae. Mayo et al. (1997)
agreed, as did Grayum (1990), who, however, added
the orontioid genera. The orontioids do not fit here
in terms of leaf type (elliptic) and petiole aeren-
chyma (type 3 only).

Bogner and Т (1991) established an ех-
panded subfamily concept, highly variable in terms
of vegetative and floral characters, that included 8
tribes and 23 genera. Included are the bisexual-

Annals of the
Missouri Botanical Garden

flowered group, the orontioids, and the African gen-
Nephthytis,
Their tribe Lasieae

era Gonatopus, Zamioculcas, Ancho-

manes, and Pseudohydrosme.
(herein subfamily Lasioideae) subtribe Draconti-
inae (plants with perigone) holds nine genera, and
subtribe Pycnospathinae (no perigone) includes
solely Pycnospatha in their Lasioideae. Superfi-
cially, the habit and leaves are similar in the Af-
rican genera, as is their possession of banded col-
lenchyma, and types I and Il vascular bundles.
However, the African genera often have laticifers
or ducts, and biforines or biforine-like raphides,
which are absent in the core lasioids as defined
here. In my opinion, Bogner and Nicolson's subfam-
ily concept is polyphyletic based on molecular and
current structural evidence.

Supporting a restricted concept of Lasioideae are
studies by Seubert (1993, 1997) describing the dis-
tinctive, ornamented lasioid seeds, and the work of
Hay (1992) on biogeography of the Lasieae that
suggests a separate and prolonged evolutionary his-
tory for this group of genera.

SUBFAMILY CALLOIDEAE

The sole genus is the circumboreal herb Calla.
This rooted aquatic has a fully expanded spathe, a
more or less uniform spadix that includes bisexual
flowers without perigone, a petiole sheath with ex-
tended apical ligule, the cordate-pinnate leaves
with higher-order parallel, arcuate veins merging
toward the margin, and petiole with type 3 aeren-
chyma. Vascular bundles are types I and IL collen-
chyma is absent, and laticifers are non-anastomos-

ng.

The cpDNA tree (French et al., 1995) confirms
its isolated position, as does its unique combination
of boreal range, plus morphological and anatomical
factors. (1991) Hotta
(1970) agreed with this circumscription. Uniquely

Bogner and Nicolson and
in the history of this genus, the consensus tree for
rbcd and matK genes (Cabrera et al., 2003) sug-
gests placement of Calla on an isolated arm be-
tween the schismatoglottids and the subfamily Aro-
ideae. Grayum (1990) had included Calla in a large
subfamily concept containing 40 genera, which are
distributed among four of my subfamilies.

The remaining 75 genera have unisexual flowers
and are monoecious. Mayo et al. (1997) considered
them to be monophyletic and sufficiently closely
related to constitute a single subfamily Aroideae
(see table 3, Keating, 2000). However, within that
arge grouping, structural data, together with the

cpDNA tree topology, and the numbers of restric-

lion site changes, provide additional support for
subfamily-level recognition for the taxa that follow.
SUBFAMILY PHILODENDROIDEAE

This subfamily includes seven tribes and 27 gen-
era. Vascular bundles are types I and II, fibers oc-
cur as phloem caps, secretory ducts are present or
absent, and laticifers are non-anastomosing. The
best anatomical character uniting this group is col-
lenchyma occurring as types B and Bi. While the
strict consensus tree for rbcd and matK genes dis-
plays unresolved relationships of the tribal group-
ings, the cpDNA tree indicates a common origin for
the included genera and provides the framework for
the sequence that follows. Together these genera
constitute the most structurally diverse subfamily.
ated

Tribe Philodendreae includes five closely re
genera of the American and African tropics, south-
Montrichardia, Anubias,
In ad-

east Asia, and Malaysia:
Furtadoa, Philodendron, and Homalomena.
dition to the cpDNA results, all are marked by a
rare character, shared by only two genera of the
tribe Culcasieae, possession of sclerotic hypoderm
in the roots (French, 1987c). In other recent sys-
tems, the five genera of Philodendreae are scattered
among various tribes and subfamilies, probably due
to structural variations. Laticifers and ducts are of-
ten present, but vascular bundles, aerenchyma, and
leaf venation and stem habit are all variable (Keat-
ing, 1997).
indicate some isolation between Montrichardia and

—

The sequence data of Cabrera et a

the other four genera.

Tribe Zantedeschieae, including Zantedeschia of
southern Africa and Callopsis of eastern Africa, has
banded-interrupted collenchyma, not a common
type. These genera are placed in separate tribes in
most schemes and they differ in diagnostic char-
acters of their anatomy: Zantedeschia lacks fibers,
has parallel intersecondaries in the leaf, elongated
raphide cells and biforine-like raphides, type III
vascular bundles, and type 3 aerenchyma. Callopsis
lacks fiber caps as well as the other characters. The
rbcd and matK sequences would support tribal-lev-
el separation. On the other hand, the cpDNA tree
suggests a close relationship.

Tribe Stylochaetoneae, including the African ge-
nus Stylochaeton, has perigoniate flowers, a char-
acter it shares with the next tribe, Zamioculcadeae.
Stylochaeton is easily distinguished from the next
two genera in having type 3 aerenchyma, biforine
raphides, and fibers absent. These two tribes, and
tribe Zantedeschieae, share the same long branch
on the cpDNA tree. Cabrera et al. (2003) show this
tribe as being closely allied to the following tribe.

Volume 91, Number 3
2004

Keating
Vegetative Anatomical Data

Tribe Zamioculcadeae contains the genera Gon-
atopus and Zamioculcas of southeast Africa. They
have fibers as phloem caps, variable collenchyma
(types B. Bi). secretory ducts present or absent, sty-
loids occasional, and elongated raphide cells. In
the cpDNA tree, the tribe is at the end of a clade
having 29 additional restriction site changes and a
number of structural differences. This is consonant
with the clustering found in the лед and matk
gene consensus tree. the
tribes Zamioculcadeae (Gonatopus and Zamiocul-
cas) and Stylochaetoneae (Stylochaeton) have been
placed in about six different subfamilies. but they

In earlier classifications.

are at home in the present concept of subfamily
Philodendroideae.

The leaf of Stylochaeton is simple while those of
Gonatopus and Zamioculcas are pinnately com-
pound. Stylochaeton has type 3 aerenchyma while
Gonatopus and Zamioculcas have only compact aer-
enchyma. Gonatopus and Zamioculcas have occa-
sional styloids. The three genera also vary in habil
but are the only monoecious genera of Araceae with
pe бышы flowers.

Iribe Aglaonemateae includes the African. gen-
era Nephthytis.
the southeast Asian and Malaysian genera Agla-

Anchomanes, Pseudohydrosme, and
onema and Aglaodorum. They have fibers, well-de-
veloped as bundle sheaths or caps. collenchyma of
types В. Bi, and Sb, and non-anastomosing latici-
fers. They have been placed in two tribes and there
are some differences to support this, including con-
temporary geographic separation, although Neph-
thytis occurs throughout the tribal range. There are
differences in leaf shape. Similarities include the
presence of type Sb collenchyma, a rare occurrence
in the Araceae, and the presence of biforine raph-
ides. Combined molecular genetic evidence and the
collenchyma development support the present con-
сері.

Tribe Culcasieae includes the tropical African

genera Culcasia and Cercestis. They have type
vascular bundles, type В collenchyma. and secre-
In the they
hypoderm with septate fibers, and resin canals, all
features shared by at least some members of the

tory ducts. roots, possess a sclerotic

tribe Philodendreae. The genera are isolated on the
same branch of trees using molecular genetic evi-
dence and appear classified together by Mayo et al.
(1997). Grayum (1990) placed them in adjacent
tribes in this subfamily, while Bogner and Nicolson
(1991) placed the adjacent tribes in subfamily La-
sioideae. Raphides, leaf shape. collenchyma, aer-
enchyma, and fibers all support their close rela-
tionship and placement within the Philodendroideae.

Tribe Spathicarpeae includes 10 tropical and

Dieffen-
Synandros-
Man-
gonia, and Taccarum. They share variable vascular
bundle form (types J. II. HI).
bundles or as bundle caps, collenchyma type B.

subtropical American genera: Bognera,

Spathantheum, Gorgonidium.

Spathicarpa,

bachia,

padix, Gearum, Asterostigma,

fibers ensheathing

laticifers with transparent contents, non-anastomos-
ing. or absent. All recent systems (Gravum. 1990:
Bogner € Nicolson, 1991; Mayo et al.. 1997) and
gene sequence evidence agree on a close relation-
ship for these genera. The presence of laticifers
with transparent contents is diagnostic.

The subfamily Philodendroideae embodies the
most diverse set of character states in the family.
and not just due to the inclusion of the huge and
character-rich genus Philodendron. Considering
this diversity, the subfamily remains coherent be-
cause of the type B collenchyma and derivative

types and the molecular data.

SUBFAMILY SCHISMATOGLOTTIDOIDE AE

This subfamily, containing two tribes and seven
genera, is recognized for the first time (Appendix
3). The plants are mostly evergreen herbs, mostly
aquatic ог amphibious with simple. pinnately
veined leaves. Their spadices have unisexual flow-
ers separated by a naked or sterile flower zone,
usually without a sterile appendix. Pollen are al-
most entirely psilate and inaperaturate.

Most. genera have representatives Borneo or
Brunet. In addition, Schismatoglottis ranges in Ma-
lavsia and southeast Asia and includes three spe-
cies in South. America. Piptospatha is found in the
Indonesian peninsula. Cryptocoryne occurs in south
India. Indochina, south China, and the Philippines,
Indonesia to New Guinea, and Lagenandra ranges
from Assam to Bangladesh.

Anatomical features common to the subfamily
usually include epidermal cells with straight-sided
polygonal walls (surface view) that are large or co-
lumnar in transverse section, and brachypara-hex-
acytic stomata with narrow subsidiary cells. Fewer
or more subsidiary cells also occur. Vascular bun-
dles are types H and HI. Ground tissue in the pet-
iole or midvein is type 3, or occasionally type 4.
The collenchyma pattern is banded or banded-in-
terrupted, approaching stranded in the Cryptoco-
ryneae. However, collenchyma strands appear not
to be the more organized type Sv strands as de-
scribed below for the subfamily Aroideae. A tran-
sitional condition, showing the capacity form
both types of collenchyma, has been detected
the schismatoglottid genus Bucephalandra (Keat-
ing, 2000, 2002).

The genus exhibits banded col-

490

Annals of the
Missouri Botanical Garden

lenchyma in the midrib and more discrete strands
in the petiole. Raphide crystals are variable and
not useful for distinguishing this subfamily or its
tribes. Pollen is reported (Grayum, 1992; Mayo et
al., 1997) as inaperturate and psilate. They report-
ed irregularly dimpled pollen in Hottarum (now in
Piptospatha) and rugulate or verrucate pollen in
Schismatoglottis.

Tribe Schismatoglottideae holds the five genera
Phymatarum, Schismatoglottis, Aridarum, Piptos-
patha, and Bucephalandra (also see Bogner & Hay,
2000).

and South America (in the case of Schismatoglottis).

They occur in Malaysia and southeast Asia,

Fibers as bundle caps are present or absent, non-
anastomosing laticifers are present, and collenchy-
ma is type B or Bi. Two pollen nuclei are present
at anthesis.

n
t at

Tribe Cn includes the Asian and
Malavsian genera Cryptocoryne and Lagenandra.
They have type Bi collenchyma that may approach
the stranded appearance of type Sv as in the sub-
family Aroideae as described above. However, they
can be distinguished from the latter. Where inde-
pendent strands appear, they may oecur in the ab-
sence of vascular bundles as well as occurring
aligned with them. Fibers are absent, as are latic-
ifers in the leaves. Three pollen nuclei are reported
in these two genera.

The two tribes were first placed adjacent to each
other by Mayo et al. (1997) in their Schismatoglottis
alliance of the subfamily Aroideae. Other recent
systems have constituted the tribes as given here,
but with separated subfamily placements. Grayum
(1990) placed the tribe Schismatoglottideae in the
subfamily Calloideae and the Peltandra alliance
and the tribe Cryptocoryneae in the subfamily Aro-
ideae. Bogner and Nicolson (1991) placed the tribe
Schismatoglottideae in the subfamily Philodendro-
ideae and the Cryptocoryneae near the end of their
subfamily Aroideae. On the basis of combined mo-
lecular genetic topologies, the two tribes exhibit
proximity of relationship. Also, anatomical features,
especially collenchyma, reflect the same transition-
al position between the subfamilies Philodendro-
ideae and Aroideae.

SUBFAMILY LEMNOIDEAE

Five genera, Spirodela, Landoltia, Lemna, Wolf-
fia, and Wolffiella, are included in subfamily Lem-
noideae. This group of small, floating plants has
type П vascular bundles, no collenchyma or latic-
ifers, but does contain raphide cells. The genera
have appeared to form an easily interpreted reduc-
tion series, in the above order, beginning with Spi-

rodela. However, the strict consensus tree of Roth-
well et al. (2004) indicates that Lemna is related at
a node distal to Wolffiella.

The lemnoids have been the subject of a recent
detailed review and structural account by Landolt
(1998). who accepts family-level recognition. All
DNA sequence data indicate that the genera are
clearly nested within Araceae. While the plants
themselves are very reduced in stature, the anatom-
ical data gathered from them are compatible with
the genera clearly being aroids. Stockey et al.
(1997) reviewed paleobotanical evidence that lem-
noid genera and Pistia may be related through the
transitional genus Limnobiophyllum that occurs in
Paleocene and Miocene strata. However, the mor-
phological distance between lemnoids and other ar-
oids as well as the molecular genetic data best in-
dicate subfamily-level recognition, and isolation
from Pistia,

SUBFAMILY AROIDEAE

This subfamily contains the remaining 8 tribes
and 36 genera of Araceae. As defined here they are
the most anatomically uniform subfamily. Most im-
portantly, all genera possess true type Sy collen-
chyma, and are the only genera to do so (Keating.
2000). This type occurs usually as subcircular in-
dependent strands always aligned with, and exter-
nal to, peripheral vascular bundles. Collenchyma
strands never appear as closely proximal phloem
caps. The genera possess types П and Ш vascular
bundles. Laticifers are usually non-anastomosing,
but occur as anastomosing in two tribes, and only
in this subfamily. This concept of Aroideae corre-
sponds exactly with the cpDNA tree, and the gen-
era emerge from a single well-resolved clade on the
rbed and matK strict consensus tree.

Until recently, the presence of articulated latic-
ifers seemed to unite a group of genera as a single
subfamily the cpDNA
tree first provided evidence that articulated latici-

Colocasioideae. However,
fer-bearing clades arose independently in the Old
World (Colocasieae) and the New World (Cala-
dieae). The tribes are not adjacent on any molec-
ular genetic tree. Earlier, Fox and French (1988)
called attention to the presence of sterols in latic-
ifers of the New World Xanthosoma and Syngonium
(tribe Caladieae here), but only sterol esters in the
Old World Alocasia and Colocasia (tribe Coloca-
In this case, aggregated anatomical data
have not been sufficient to separate these groups,

sieae).

an illustration of the difficulties of using structural
data in isolation
ribe Thomsonieae includes Amorphophallus of

Volume 91, Number 3
4

Keating
Vegetative Anatomical Data

Africa, southeast Asia, Malaysia, and northeastern
Australia, and Pseudodracontium of southeast Asia.
Their leaves show tetrahedral branching at the apex
of robust. erect petioles, reticulate venation in in-
tercostal areas. and non-anastomosing laticifers.
The genera have been traditionally recognized as
forming a tribe.

Tribe Caladieae includes 11 genera: Hapaline,

Syngonium, Xanthosoma, Chlorospatha, Ulearum.

Filarum, Zomicarpella, Caladium, Scaphispatha,
Jasarum, and Zomicarpa. They are South American
except for Hapaline, which occurs in southeast Asia
and Brunei. Phloem fiber caps are common, raph-
ides are variable, including biforines, and anasto-
mosing laticifers are present. The genera of this
tribe are often divided into two tribes (Bogner &
1991; Mayo et al., 1997;

1990, in part), but molecular genetic evidence pro-

Nicolson, and Grayum,
vides no support for further separation or recogni-
tion of a tribe Zomicarpeae.

The tribe Arisareae contains Ambrosina and Ar-
isarum of the Mediterranean region. They have type

II vascular bundles, non-anastomosing laticifers,
and type 4 petiole aerenchyma. The two genera are
often divided into separate tribes but the cpDNA
tree provides no support. The two genera appar-
ently share a close common ancestry with the next
tribe.

Tribe Peltandreae is interpreted here to include
five genera: Peltandra of eastern. North. America,
and from Madagascar: Typhonodorum, Colletog yne.
Carlephyton, and Arophyton. Leaf intersecondaries
are numerous and parallel, raphides are biforines
and biforine-like cells, laticifers are non-anasto-
mosing, and petiole aerenchyma is type 3. The geo-
graphic disjunction is less puzzling when consid-
ering fossil evidence. Ancestors of Typhonodorum
were in North America (Tennessee) during the Eo-
cene, indicated by specimens named Philodendron
Dilcher and Daghlian (1977). They
were later considered as belonging in tribe Peltan-
dreae near Typhonodorum by Mayo (1991). The
(2003) suggest a separation
of Typhonodorum from Peltandreae, but on the ba-

limnestes by

trees of Cabrera et al.

sis of microscopic structural evidence, no further
rearrangement is undertaken. Together the five gen-
era share a number of leaf characters including bi-
forine raphides and biforine-like cells, non-anas-
tomosing laticifers, and type 3 aerenchyma. There
are some variations in histology but not sufficient
to recognize separate tribal status.

Tribe Pistieae comprises pantropical floating
plants of the genus Pistia. Leaf aerenchyma is type
3, collenchyma forms types С and Sv, biforine raph-
ides are present, and laticifers are absent. In spite

of the distinctive aquatic life-adapted features of
the genus, it fits into the Aroideae according to mo-
and its histology, sum-
The

type Sv collenchyma strongly confirms this place-

lecular genetic evidence,
marized above, is typical for the subfamily.

ment. There appears to be no support for separate
TE status as proposed by Takhtajan (1997).
ribe Arisaemateae consists of the genera Ari-
Asia, and. North
America, and Pinellia of eastern Asia and Japan.

saema, widespread across Africa,

Both share leaf secondary venation having brochi-
dodromous loops, raphide cells elongate with mul-
tiple or overlapping bundles, and laticifers non-
| broad array of
2004) . and
the леа and matK gene consensus tree, suggests

anastomosing. The presence of а

raphide types in these genera байды!

an affinity with the following tribes Areae and Col-
осаўтеае.

Tribe Areae now contains seven genera that ex-
tend from the Mediterranean region to India and
Sri Lanka, Africa, Ma-
and northeastern They are: Ty-

southeast Asia into China,

laysia, Australia.
phonium, Theriophonum, Biarum, Arum, Eminium,
Dracunculus, and Helicodiceros. The plants are tu-
berous and have similar anatomy that includes type
3 ground aerenchyma, type II vascular bundles.
leaf venation with ascending secondary veins and
brochidodromous loops, reticulate fine venation,
non-anastomosing laticifers with transparent con-
tents, and raphides occurring in elongated cells
(Keating, 2004). A likely close relationship among
these genera is supported by DNA sequence evi-
dence.

Africa, south and

east Asia, Malaysia, and northern Australia. The six

Tribe Colocasieae occurs in
genera are: Ariopsis, Alocasia, Remusatia, Coloca-
sia. Steudnera, and Protarum (Seychelle Islands).
Shared structural features include parallel and
merging leaf tertiary veins, variable patterns of leaf
aerenchyma, laticifers non-anastomosing or anas-
tomosing. and biforines often present.

Genera of Colocasieae have been variously
placed. They were regarded as a coherent grouping
by Grayum (1990), except that he placed Artopsis
in a different subfamily. Bogner and Nicolson
(1991) placed the six genera among four separate
tribes. The cpDNA tree as well as anatomical evi-
dence yield no rationale suggesting separate tribal
status for any of these genera, except that half pos-
sess anastomosing laticifers and half non-anasto-
mosing, a circumstance not considered to influence
tribal affinities in previous classifications. The rbed
and matK consensus tree is equivocal, placing Al-
ocasia оп a separate branch. If these genera oth-
erwise prove to constitute a natural group, an in-

492

Annals of the
Missouri Botanical Garden

vestigation regarding evolution and relationship of
laticifer types among the genera should be under-
taken.

In the recent past, an accelerating tempo of ad-
ditional data is yielding closer approximations to
the truth. Family-wide data surveys by a number of
workers have been instrumental in sharpening our
understanding of this complex and ancient family.
As reviewed by Mayo et al. (1997), Croat (1998),
and Keating (2002, 2003), these results have clar-
ified our understanding of relationships within the

amily, and the family’s place among the monocots.
The Araceae are ready for developmental surveys
that should produce major advances in our under-
standing when integrated with DNA sequence re-
sults from all available genomes and with data on
phenotypic structure and secondary chemistry.

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Dilcher, D. L. 1. 1977, Inve A from
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& — . 198 1d.
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Hotta. M. 1970. A system of ia nn Araceae in Japan
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2000. Collenchyma in pea eae: Trends and re-

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mous age ko ara Borntraeger, Berlin.
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Mavo, revision ol кш subgenus
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Araceae. Taxon 33: 680-690.

8. History of aroid systematics. Aroideana 10:

~
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23-30.
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. Stoc ne y. 2004. Molec ша? phylogenetic relationships
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Molec. Genet. Evol. :

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5

Schott, Н. 1860. Prodromus Systematis Aroideanum. Con-
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Seubert, E. . Die Samen der Araceen. Koeltz. Ko-
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1997. A ee ar dede study of seeds of Lasieae

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Stockey, R. X., C. L. Hoffman & í 1997.
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ж phylogeny of Lemnaceae. Amer. J. Bot. 84: —

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Takhtajan. A. 1997. Diversity and Classification of Flow-
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APPENDIX l. Revised classification of the genera of
Araceae.
Family Araceae Juss., 1789

Subfamily Gymnostachydoideae Bogner & Nicolson, 1991
E. 1

Gymnostachys R. r.
M Orontioideae Mayo, Bogner & P. C. Boyce,
19
8 Orontieae R. Br., 1827

Orontium
Tribe Sy 106 n ae Engl..
Lysic hiton Schott
Symplocarpus "Salisb.
E Pothoideae E ngl.,
Tribe Patios ае Bartl., 1830
Potho
Pedicellarus im* M.

Pothoidium* Schot

1876

~

1876
Hotta
tt

‚ 1876

an
Alloschemone* Se ‘hott
Epipremnum Schott
Amydrium Schot
Kunth

Heteropsis* 1

1876

W Lasioideae E ngl.,
Јуғоѕр i

А Т Нау
Рус 1 Thorel.
Dracontit
Jraconti oides Ti
жш: Calloideae Endl..
aL
Suhail Philodendroideae ke M
ribe Philox endreae p^ 1856
Малы еы На Cri
{nubias Schott

1837

1876

~
=
=
=
LI
A
>
=
=
=
D
=
^
a

‘ho
Tribe Zantedeschieae Г чыё 1687
Zantedeschia Spren
Callopsis Engl.
Tribe Stylochaetoneae Schott, 1850
Stylochaeton Le pr.
Tribe Zamiocule ad ae Schott ex Engl..
Gonatopus Hook.
Zamioculcas Se a

Iribe Aglaonemateae E ngl., 1876
Vephthytis Schott
Inchomanes Schott
Pseudohydrosme* Engl.
lglaonema Schott
гени Schott
Tribe Culcasieae Engl., 1887

)eauv.
Cercestis Schott

Tribe Spathie A ae Schott, 1856
Bognera Mayo & Nicolson
Dieffe тасма Schott
Spathantheum Schott
Gorgonidium Schott
Sy иа Engl.
Gear * N. E. Br.
tmd Hook.

sterostigma Fisch, & C.

Mangonia* Schott

Taccarum Bron

n Brongn.
Subfamily Schismatoglottidoideae К.

A. Mey.

=

-

nov.
Tribe Cryptoc 2 ae Blume, 1836
Cryptocoryne Visch.
Lage nandra kn
Tribe Schismatoglottideae Nakai,
Phymatarum M. Hotta
Se Eco, rg Zoll. & Moritzi

Iridarum Ridl.
Piptospat de x |
Bucephalandra* Schott

fi S
Subfamily Le mnoide ае Bab. 1843
Jiro т d.

1943

870

Spl idela* S E

Landoltia* . Les & D. J. Crawford
Lemna L.

Wolffta* Hor

Wolffiella* M Im.) 13

Subfamily Aroideae Arn.,
Tribe Thomsonieae Blume, i

C. Keating, subfam.

494

Annals of the
Missouri Botanical Garden

sl ut
Pseudodraco
Tribe Caladicae Es о
Hapaline Schott
Syngonium Schott
Xanthosoma Schott
жерын Engl.
Ulearum Engl.
Fila nat Nicolson
1 m Post & Kuntze
adiu 'ent.
© vapliphu* pus
junting

. E. Br.
1832

Arisarum

Tribe Pe 3 Engl., 1876
Peltandra Raf.
ood Schott
Collet e Buchet
Carle, n id
rophyton Jui

Tribe Pistieae Ric h, 1831
Pistia L.

Tribe Arisaemateae Nakai, 1943

. 1828

Гей ши Blume
Biarum Schott
Art

um
Eminiu um yes ) Schott
racunculus*
Helicodiceros S« re
Tribe Colocasieae (Schott) Brongn.,
Ariopsis Rojas
Alocasia (Schott)

E

1843

G. Don

Protarum* Engl.
*Genera not included in the cpDNA survey of French et
al. (1995
APPENDIX 2. Definitions of character state typology.

De EN dese d of vegetative anatomical charac-
ters can be found in Keating (2002). For the cha
states disc ussed he re, the following typology applie s. Oth-
er terms not further defined below are used in the usual
sense of contemporary anatomy texts.

Collenchyma. T
or near the phloem of a vascular bundle. Type B: a pe-
rimeter band of collenchyma that ensheaths the abaxial

aracter

С: a strand that forms a cap over

side of a midrib or petiole. Type Bi: collenchyma bands
that are interrupted infrequently. Type Sv: collenchyma
strands arranged around the perimeter of a midrib or pet-
iole, and aligned on the same radius as the outer vascular
bundles. They ər not close enough to
vase lap bundles to be considered caps. Type Sb: collen-
chyma strands near an organ perimeter that are arranged
between vascular bundles, or not in relation to vascular
bundles.

Vascular bundles. Type I: broad bundles with semi-
circular strands of xylem and m m se inii d by a wide
straight boundary. Several files of metax ells are pre-
sent. Type ЇЇ: a narrower bodie ну EA boundary
between 1 xyle m and phloem. Only a few metaxylem ce lls
П: a bundle шош! by a single
narro

are either circular ¢

are present.
large, persiste nt, protoxylem lacuna opposite i
phloem strand.

Aerenchyma cavities. Type 3: numerous large cav-
ilies se aii 'd from each other by uniseriate partitions.
Type 4: a few la arge | cavities present separated by bi- or
multiseriate partiti

Raphides. Biforines are spindle-shaped cells with
lignified walls, bearing a single raphide bundle. Cell ends
usually bear thin-walled papillae. Biforine-like cells
have thinner, non-lignified walls and undifferentiated cell
ends

APPENDIX
Schienatnelattiiollens R.

Description of оне ily
. Ke ating, subfam. nov.

Haec subfamilia a ceteris subfamiliis Arac earum habitu

thecis truncatis cornutisve atque pollinis granis inapera-
turatis plerumque psilatis distinguitur.

Plants occasionally terrestrial, mostly aquatic or am-
phibious, stems rhizomatous, mo stly epigeal or dec 'um-

aticifers non- е
{Оп le aves. Infloresc

, lhecae truncate or horned, de.
hiscent with apical pore. Pollen 5 mostly psi-
ate. Ovary é

discoid or capitate. Fruit a bern or sy
soid, embryo axile, straight, elongate. 1 present,

l-locular, ovules

often copious.

SYSTEMATIC OCCURRENCE
OF RAPHIDE CRYSTALS IN
ARACEAE!

Richard С. Keating?

ABSTRACT

The presence of idioblastic cells bearing calcium oxalate raphide crystals is a n character for Araceae. This

light microscopical survey of vegetative organs, mostly
ami E او‎ the
. Cell t
be simple, ое This у
though each of the
are found only among the unisexual-flowered g

Key words:

r кз foam -overlapping.

leaf and petiole tissues, of 104 ou
presence of sever
ae may be unmodified with
gated, tubular, artic sone: d.

of 106 recognized genera «
al distinc ‘tive raphide crys \
respect to өү кес, cell shapes, or may һе
spindle-shaped, or biforine-shaped. Crystal |

iation is posted against a new classification of the family. Al-
nine subfamilies has a en оне ‘tion of types, trends of specialization are obscure.

Biforines

Anatomy, Araceae, calcium сн prem idioblast, raphide.

Raphide crystals are most commonly encoun-
tered among monocotyledonous families of flower-
ing plants (Dahlgren & Clifford, 1982). For the Ar-
aceae, raphide presence is a defining character
whose absence has been useful in, for instance, ex-
cluding the Acoraceae from the family (Grayum,
1987). However, it is also interesting to note that
raphides are not reported to occur within Alisma-
tiflorae (Dahlgren & Clifford, 1982;
1982). The included families are now believed to

be the nearest neighbors of aroids in a recent or-

Tomlinson,

dinal classification (Angiosperm Phylogeny Group
(APG), 1998).

ceae include most of the 103 genera listed in Mayo

As presently constituted, the Ara-

et al. (1997) plus the five genera of Lemnaceae,
vielding a current total of 106 genera (Table 1). The
lemnoid genera are clearly embedded. within the
family based on DNA sequences (see Keating.
2002, 2003, 2004 this volume).

This investigation of araceous raphide crystals is
aimed at enumerating the variety of types of raph-
ide-bearing cells and crystal bundles as they occur
in vegetative structures in the family. Secondly, the
resulting typology was plotted against a contempo-
rary classification (Keating, 2004) in order to assess
potential evolutionary trends or systematic concor-
dance.

Knowledge of this idioblastic cell type in the Ar-
aceae began with the description of biforines by
Turpin (1836). Since then, various systematic ac-
counts of raphides have been published including

those of Buscalioni (1895-1890: Soler-
eder and Meyer (1928: 16 genera), and Genua and
Hillson (1985: 14 genera).

chemistry of raphides has been subject to a few

| genera).
The development and
detailed studies, and the subject has been reviewed

(1980).

raphides are found to be monoclinic crystals of cal-

by Franceschi and Horner In each

case
cium oxalate monohydrate (whewellite). They ap-
pear to occur universally as bundles of needle-
shaped crystals within vacuolar crystal chambers of
idioblastic cells. Sakai et al. (1972) and Cody and
Horner (1983) described deep grooves on raphide
surfaces of Colocasia, Alocasia, and Xanthosoma.
In addition, such crystals may also have backward-
oriented surface barbs capable of increasing dam-
age to the mouths of grazing animals.

MATERIALS AND METHODS

Samples of vegetative material representing 106
genera were prepared for a general light micro-
scopic (LM) histological survey. Only Bognera and
Landoltia (Lemnoideae) are missing. About 380
species, mostly liquid-preserved, were examined
for general histology of leaf lamina, petiole, stem,
and root, and are listed in detail in Keating (2002).
Therefore, the specimens examined list (see Ap-
pendix 1) here is only representative. For some
specimens, microtechnique was accomplished us-
ing conventional paraffin techniques (Ruzin, 1999;
Berlyn & Miksche, 1976). For others, hand sections
were produced that were stained in cresyl violet

! [ am grateful, in particular, to Josef Bogner and Thomas Croat, who Жан numerous samples for this study. Also

thanks to David Boufford and Simon Mayo

for specimens, to Su

uzanne Eder К aum assistance, and to Graduate

Studies and Research, Southern Illinois University at Edwardsville, for grant supp

2 Missouri Botanical Garden, P.O. Box 299, St.

Ori
Louis, Missouri 63166-0299, U.S. A richard.keating@mobot.org.

ANN. Missouni Bor. GARD. 91: 495—504. 2004.

496 Annals of the
Missouri Botanical Garden

DÀ р.

o Y,
924624 i = ane 19M.

Figure 1. | > rmal leaf sec к showing raphide crystal-bearing cells. —A. Monstera е Simple raphide cell

re wide crystal packet. —B. Lysichiton oe Simple ach de cell suspended within spongy mesophyll.
—C. Anubias halin Elongated cell single packet. —D. Spathantheum orbignyanum. Simple raphide tube with two
short crystal packets. —E. Anthurium роГух un Tubular ce " containing oblique overlapping crystal packet. —F. Pedi-
cellarum paiei. Elongate raphide cell conte ee М ove NADIE helical raphide packet. Above, note rows of rhombohedral
crystals, rare in the family, along the vascular и Н. 1 riedeliana. G. 0 уер ulated raphide tube.
—H. Sinuous articulated raphide tube. Scale lin E ` = 200 pm: В = 100 um: С. H = 500 um.

>

Volume 91, Number 3
2004

Keating
Raphide Crystals

acetate and wet-mounted in calcium chloride so-
lution. With its high refractive index, calcium chlo-
ride is an excellent mountant (Herr, 1992; Keating,
1996) for observing general histology. However,
with time, calcium oxalate crystals will erode in its
presence. Because of the focus here on crystals,
hand sections were also wet-mounted in glycerine,
a mountant in which crystals appear to be archival.
However. use of glycerine or other alcohols. pre-
cludes permanent staining of cell walls or contents.
Initial orientation to observing calcium oxalate
crystals is improved by using polarized light. This
type of crystal can also be detected and seen clear-
ly with bright field LM. One stops down the sub-
stage diaphragm to a point where diffracted light
from the crystals provides sufficient contrast for de-
tection.

The data are arrayed in Table 1 according to a

—

new family classification sequence (Keating, 2004
that the
available DNA sequence studies (French et al..
1995: cpDNA
prep.: rbed and так genes; and Rothwell et al..

was influenced by structural data and

restriction sites; Cabrera et al., in

2004: chloroplast trnL-trnF intergeneric spacers).
The subfamilial and tribal names recognized in the
list are adopted as discussed in Keating (2004).
Twenty-one genera not included in the cpDNA sur-
1995) were easily inserted here
(1997)

vey (French et al.,
on the basis of placement by Mayo et al.
and by the general anatomical concordance.

OBSERVATIONS

A surprising variety of crystal-bearing cells and
crystal bundle configurations was encountered as
described and illustrated below. It is possible to
consider the cell characteristics and the crystal-
bundle characteristics independently. Also, it was
discovered early that the greatest diversity of types
occurs in the lamina, with progressively less com-
plexity occurring in ground tissue of the petiole,
stem, and root. Roots usually have only the un-
modified (U) type. Therefore, this survey emphasiz-
es the lamina and, in so doing, | believe no unique
types are left unaccounted for. Examination of the
petiole may add the U type if it is not encountered
in the lamina. Almost universally, some raphides
are present in all organs examined, even if rarely
encountered.

Within raphide-bearing cells, cytological struc-

ture and staining behavior suggest the existence of

wide variation in the amount and type of com-
pounds that are included within or surrounding the
crystal chamber. Often these other contents are
deeply staining or nearly opaque. obscuring the

crystals themselves. Most frequently, crystals are
not obscured by other materials. This chemistry was
not further investigated in this study.
CRYSTAL AND CELL TYPOLOGY

Unmodified (U) cells are irregularly shaped, and
usually considerable cytoplasmic coexists
with the crystal bundles (Fig. ТА. B). U
widespread in the family, not always common, and

space

cells are

they appear to be missing in some genera. In roots
and stems, which have larger parenchymatous tis-
sue cells, these isodiametric or irregular crystal-
bearing cells often vary little in shape and size from
neighboring parenchymatous tissue, the only idio-
blastic feature being the inclusion of crystalline
contents. In leaves, U cells are less common than
the more specialized types described below. Within
mesophyll tissue they are larger than typical me-
sophyll parenchyma cells but remain thin-walled
and contain one raphide bundle. Crystal bundle
3X that of bundle width.

Styloids (S), also called pseudoraphides by Dahl-
gren and Clifford (1982), are monoclinic crystals of

length is 2—

raphide length, but are broader. They occur indi-
vidually within cells or may be aggregated within
bundles as coarse raphides. The 5 type occurs rare-
ly (Anadendron, Gonatopus, Zamioculcas, Amorpho-
phallus) and is never common.

Wide cells (W) often approach spheroidal in
shape and usually contain a broad raphide bundle
where its width exceeds. bundle
length (Fig. LA). The cells often are similar to type
U but are defined by a combination of cell shape
They

genera appearing early in the classification (Table

approaches or

and bundle width. appear more frequent in
1) and are quite uncommon in the subfamily Aro-
ideae.
Elongated cells (E) are about 3X the length of
usual crystal bundles (Fig. 1C). and they may in-
clude 2 or more bundles, coded as (2+) (Fig. 1D).
E cells may contain oblique-overlapping bundles
(Ov). which may occupy most or all of the length
of the cell (Fig. ТЕ, К). Ov crystals may appear to
be helical in orientation or the crystals are oblique-
ly stacked in only one plane. Elongated cells are
mostly concentrated in subfamilies branching at
nodes earlier than the Aroideae. This cell type, as
well as the preceding raphide types. was referred
to as "non-defensive raphide idioblasts" by Sunell
and Healey (

Tubular cells (T) are 4X or greater in length than
the included crystal bundle (Fig. They are
most common earlier than the Aroideae but also

occur in that subfamily. While not as common as

498

Annals

of the
Missouri Botanical Garden

Table 1. Revised classification of Araceae! showing raphide cell and crystal types encountered in each genus.

Family, subfamily,
or tribe

Genus

Raphide type?

ACORACEAE
ARACEAE
Gymnostachydoideae
Orontioideae
Orontieae

Symplocarpeae

Pothoideae

Pothoeae

Monstereae

Lasioideae

Calloideae
Philodendroideae

Philodendreae

Zantedeschieae

Stylochaetoneae
Zamioculcadieae

Aglaonemateae

Culcasieae

Spathicarpieae

Acorus
Gymnostachys

Orontium
Lysichiton
Symplocarpus

Pothos
Pedicellarum
Pothoi idi um

onstera
Allosc 'hemone

Heteropsis

Cry tosperma

La
Anaphyllum
Urospatha
Anaphyllopsis
Pyc ii cod a
Drac

Drac 1

Calla

Montrichardia
Anubias
urtado
Philodendron
oe
Zantedeschia
Callopsis
Stylochaeton

Synandrospadix

(—)
U, E: 2+

U, E: 2+
U, V. E
U, W, Sb

a tae Ov

E:

U, T; Ov 2+

U, W, E: Ov 2+, Sb
U, W, E: Ov, Sb

LE
Ü W, E: Ov 1-24
E: M
(S), U, 105 2+
V. Е

U. E: Ov, Sb, B
U De

U, E: Ov, Sb, (B)
U

U, ET

Volume 91, Number 3 Keating 499
2004 Raphide Crystals

Table 1. Continued.

Family, subfamily,
0

r tribe Genus Raphide type?
W, E: 2+, B
a U, W, E: 2+
Asterostigma U, Ta
Mangonia U, W, E: Ov 2+
Taccarum U, W, E: 2+, Ta, (Sb)
Schismatoglottidoideae
Cryptocoryneae Cryptocornye U, W, E: Ov 2+, Sb
Lagenandra U, WE: Ov
Schismatoglottideae Phymatarum U, W, E: Ov
Sc hismatoglottis U, W, B
Aridarum U, (В)
Piptospatha U, E, B
Bucephalandra U, W, Sb
Lemnoideae Spirodela U, E
Landoltia
Lemna U, E: Ov, Ta
Wolffia E?
Wolffiella E?
Aroideae
Thomsonieae Amorphophallus S JU. Es 2+
Pseudodracontium U, W, E: Ov
Caladieae Hapaline О, W. B
Syngonium U, W, B
Xanthosoma U, W, (E), B
Chlorospatha U, Sb
Ulearum U, ET: Ov
Filarum „Ж:
Zomicarpella U, ET: Ov 2+, B
Caladium
Sc ee U, B
Jasaru
A nis UW. bs 2, В
Arisareae Ambrosina W, E: 2+
Arisarum U, E
Peltandreae Peltandra U, M. B
0 U, B
Collet U, B
5 U, V. Sb. B
Arophyton U, Sb, B
Pis Pistia U, Sb. B
jos mateae Arisaema W, T: Ov 2+
iir UE: 2+
Areae Typhoni U, W, ET: Ov 2+
P U, E: Ov 2
Biarum U, ET: 2+, Ta
Arum U, W
Eminium U, E: Ov 2+
Dracunculus U, W, E: 2+
Helicodiceros U, ET: Ov
Colocasieae Ariopsis U E: 24B
Alocasia U, W, ET: 2+, Sb, B
Remusatia U, WE: 2
Colocasia U, B
Steudnera U, W, E: 2+
Protarum ULB
EG laşsjhcation based on Keating (2004).
2S = styloid; U = unmodified cell with single raphide bundle: = wide cell usually containing wide raphide
bundle; E — elongated cell; T — tubular cell; Ta — articulated n sb = thin-walled spindle-shaped cell; B =
biforine; () = mal: 2+ = two or more bundles per cell; Ov = oblique overlapping, usually eds crystal

bundle.

500

Annals of the

Missouri Botanical Garden

LN

~ T Ф we
кыл. P Y

4 un s

Figure 2.

Raphide cells in leaf and petiole sections.
sophyll, showing elongated raphide cells

. Synge

Anubias barteri. Leaf paradermal section, spongy me-
‘ells. —1 nium
cells arranged randomly in spongy mesophyll. —C. Pistia stratiotes. Leaf base
raphide suspended across aerenchyma partition. —D, E. Philodenc
ing detached biforine cell. Note very thick

angustatum. Leaf paradermal section showing three biforine
] tes. |
re

transverse section showing biforine

m bipinnatifidum.—D. Petiole center section show-

wall and terminal orifices through which raphide crystals can extrude. —

К. Midrib transverse section showing thick-walled biforine suspended by oblique attachment to walls of aerenchyma

Volume 91, Number 3 Keating
2004 Raphide Crystals

elongated cells, both types are equally likely to DISCUSSION
possess multiple bundles or oblique overlapping
bundles. A general perusal of anatomical literature sug-

Articulated tubes (Ta) are the rarest type found
in the family, being only in Asterostigma and Tac-

gests that raphide (and general oxalate crystal) di-
versity in Araceae is exceeded nowhere else in the
carum (Spathicarpieae). Lemna (Lemnoideae), and plant kingdom. But discerning its meaning and
Biarum (Areae). Each cell of a chain contains one trends is another matter. No correlation matrix was
crystal bundle. They are found as straight lines of meaningful using this data because of some inher-
cells (Fig. 1G) or taking a highly sinuous path (Fig, ent difficulties. First, although the typology listed
1H), in either case coursing randomly through the in Table 1 can be consistently applied for purposes
mesophyll as seen in clearings or paradermal sec- of recording presence of character states, the ty-

tions. In the case of Lemna, articulated cell chains Pology may be subject to some variation. Second,
are shorter than found in larger-leaved genera. the depth of sampling within genera is quite vari-
Spindle-shaped (Sb) cells are thin-walled, may able. Third, attempts to make tables where states
be straight-sided, or have side-walls tapering to- are plotted against tribes produced very little visi-
ward both ends (Fig. 2A, G, Н). Ends are usually ble systematically interesting variation. Fourth, the
rounded. Sb cells may be embedded within various degree to which some cell and crystal types may
types of parenchyma (Fig. 2F). Frequently they are be precursors to other types, either ontogenetically
found within aerenchyma where they may take sev- ©" phylogenetically, is unknown. For example, the
eral orientations: (a) parallel to and embedded WO Crys stal cells appearing in Figure 2A may rep-
within an air-space partition, (b) orthogonal to air- resent developmental stages. Fully expanded tis-
space partitions with the ends pointing into adja- — 5H€5 were sampled whenever possible, but crystal-
cent air cavities, or (c) they may be attached by one liferous cells may differentiate at different rates.
end with the other entirely suspended within an air When plotting the occurrence of the crystal types
cavity (Fig. 2G, Н). Sb cells are most frequently versus subfamilies (Table 2), it is difficult to discern
found above the lasioids but are also found within а marked pattern however useful these types may
Symplocarpus, Cyrtosperma, and Calla. They grade be for generic diagnosis, singly or in combination.
e The U type remains common in all groups and
Biforines (B). These cells are the same basic Seems lo be the basic type in the family. The W
shape as the Sb cells but differ in having lignified — type is widespread but never dominant. It appears
cell walls, as described by Turpin (1836). They are 10 be least common in the Aroideae. Elongate (Ё)
called “defensive raphide cells” by Sunell and cells seem somewhat more common in the less spe-
Healey (1985). These cell walls reach their thickest cialized genera. Tubular (T) cells are widespread
in Philodendron subg. Meconostigma. The cell ends but not common. No trend is discernable. Also, the
are usually, but not always, modified to include 2+ crystal condition that especially marks lasioids
thin-walled papillae (Fig. 2C, D) through which is widespread and shows no real trend. Oblique-
raphide crystals are rapidly extruded when the side overlapping (Ov) crystals are markedly common in
wall is deformed (see Middendorf. 1983: Sunell & the Pothoideae, but remain present in unisexual
Healey. 1985). As with Sb cells, biforines may be subfamilies. They may be considered an early spe-
oriented across aerenchyma partitions (Fig. 2B, C), — cialization that is retained. Articulated tubes (Ta)
or attached by one end and suspended within an аге rare and found in the Philodendroideae (Aster-

air cavity (Fig. 2E). No biforines are found in Sub- ostigma and Taccarum) as well as in Biarum of the
families appearing at lower nodes than the Philo- Aroideae. It seems likely that crystal cell articu-

—

dendroideae in Table 1, that is, none are present lation is independently developed in the two sub-

within the bisexual or hermaphroditic genera. They families, and its selective value is unknown.

reach their best development in the Philodendro- The thin-walled spindle-shaped cells (Sb) occur
ideae where they are well represented in all six early in the family and are possibly derived from
tribes. the U type where less cell wall expansion encloses
te
| germ . —F. Carlephyton glaucophyllum. Leaf parade rmal section with spindle-shaped cell in аат tiss

. Alocasia a Petiole transverse section showing aerenchyma partition with two spindle-shaped cells ai "m
" one end. —H. ee lindleyanum. Paradermal section showing two sp i wa shaped аг кте into
aerenchyma cavity. Scale lines: A, C, E-H = 200 um: B = 300 um; D = 100

Annals of the
Missouri Botanical Garden

502

Table 2.

Occurrence of raphide cell and crystal types in subfamilies of Araceae.!

Raphide cell or crystal type?

Subfamily U W E 2+ Ov T Ta Sb B S
Gymnostachydoideae 1/1 (—) 1/1 1/1 (=) (=) (=) (=) (=) (—
Orontioideae 3/3 2/3 2/3 E (—) (=) 1/3 (=) (=)
Pothoideae 14/16 3/16 13/16 3/16 16/16 3/16 (=) (=) (=) 1/16
Lasioideae 9/10 6/10 9/10 7/10 5/10 1/10 (=) 2/10 (—) (=)
Calloideae 1/1 (—) (—) (—) (=) (—) (=) 1/1 =) (—)
Philodendroideae 24/26 12/26 16/26 12/26 6/26 2/20 1/270 6/260 13/26 (—)
Schismatoglottidoideae 9/9 5/9 4/9 1/9 3/9 (=) (=) 2/9 2/9 (=)
Lemnoideae 2/4 (—) 2/4 (—) 1/4 (—) 1/4 (—) (—) (—)
Aroideae 34/38 11/38 20/38 18/38 8/38 6/38 1/38 5/38 17/38 1/38

! Number of genera with character/number of genera in Cd

? Raphide cell and crystal type codes as given for Table

a developing crystal bundle. Otherwise, no trend is
visible. Biforine (B) cells are usually found in gen-
era also containing Sb cells and are probably de-
rived from this basic spindle shape by lignification
of the walls and development of terminal papillae.
They are not found in the first five subfamilies, but
only in Philodendroideae and later listed genera.
Therefore, the biforine form demonstrates the best
apomorphic state transformation of any crystal cell
type within the family. Types Sb and B tend to as-
sociate with aerenchyma having large air cavities.
They are the only types that traverse partitions.

This is the first study to catalog the array of raph-
ide cells and bundle configurations from a nearly
complete generic sample of the family. It has been
noted that frequency and distribution of raphides is
not uniform within a genus or a species, often not
even within a single organ (cf. Sunell & Healey,
1985). Therefore those aspects could not be ratio-
nally addressed in the limited sample available for
a broad generic survey. The array and distribution
of types observed here can provide a background
for further study of many aspects of the biology of
crystals in the family. Variations include those of
texture, bundle size, shape, membrane system, and
chemistry of inclusions within the membrane.
Clearly, techniques in addition to LM will be need-
ed in generating data regarding membranes, ontog-
eny, and chemistry.

Finally, I should note that rhomboids, druses,
styloids, and crystal sand show some variations in
form and distribution in the family and should be
similarly investigated. The abundance of all calci-
um oxalate crystal types in the Araceae in various
forms and configurations, and the ease with which
numerous aroid genera can be grown, make the
family an excellent choice for analytical work on
crystal ontogeny, functioning, and evolution. In

spite of hypotheses proferred regarding the function
of caleium oxalate in plant tissues (cf. D'Arcy et

—

al., 1996), our understanding of the evolution of
crystals and their function remains largely specu-

lative.

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бы M & H. T. Horner. 1983. Twin raphides in the
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lulaire des feuilles dans un certain nombre d’espéces
végétales appartenant à s famille des Aroidées. Ann.
Sci. Nat., Partie Bot. II. 6: 5-27.

1836. Observations sur les Biforines, or-
s véscicles du tissu cel-

APPENDIX 1.
listed per genus.

Specimens examined, one representative

corus calamus L., Boufford 18710, Missouri (MO):
lodo pe Sa ‘hott, — 1767, cult. (М); Agla-
onema brevispathum Engl., M); Alloschemone occi-
dentalis (Poepp.) Engl. & bse, Sakuragui 1050, Brazil.
cult. M ): Alocasia cuc Шаа (Lour.) G. Don. )
Ambrosina bassti
norat Aike rand (Engl.) Engl.
ч” g. Madagascar, cult. (М); Amorphophallus kon-
K. ч ati 2089, cult. Illinois; Amydrium me-
dium (Zoll. & Morr.) ‘Nic olson, Bogner 433, Tatiana. cult.
(M): yt microstachyum (de Vries & Miq.) Back-
4, cult. (M); 5 amer-
icana (Engl. A. 4. Hay 2811, French Guiana, cult.
(M); Anaphyllum beddomei Engl., Blasco s.n., S. India,
cult. (M); Anchomanes welwitschii Rendle, as 69773,
Gabon, cult. (MO); Anthurium polyschistum R. E. Schult.
& Idrobo, cult. (M); Anubias barteri Schott var. nana
(Engl.) Crusio, Bogner 1301, cult. baron Aridarum bar
| › y. Bogner 1400

wak cult. (M); Ariopsis elio: J. E Bogner 1481,
cult. (M); Arisaema кие h Schott, cult. М; Arisarum
vulgare Targ. Tozz., cult. (M): Arophyton buchetii Bogner,
Bogner 207, Keehn ar, cult. (M); Arum italicum Mill.,

er & Alderw ra ond Pu

cult. (M); Astertstigena riedelianum Kuntze, Harley 18535,
Brazil: Bahia, cult. К.

Biarum tenuifolium (L.) Schott, 5. Mayo, cult. (М); Bu-
cephalandra motleyana Schott, Бат 1366, cult. » P

Caladium plowmanii Madison, Plowman et al.
Ecuador, cult. (SEL); Calla par L., Boufford ior
Ontario ( T Callopsis volkensii Engl., Bogner 21
); Carlephyton glauc opium Bogner, Вог.
пег 167, М on y ar, cult. (M); Cercestis congensis Engl.,
M); 5 lng (K. Krause)
, 23- эң cult. (SE Colletogyne perrieri
Bue p uiu 165, Madagascar, cult. (M): Colocasia fal-
ax Schott, Bogner 1139, uan cult. (M); Cryptocoryne
pontedenifolia Se hott, Ворт г 1093, Sumatra, cult. (М);

Cyrtosperma johnstonii
Jieffenbachia oerstedii Schott, Croat 42645, Honduras
MQ); Dracontioides desciscens Engl., Storr 075, cult. (М);
Dracontium spruceanum (Schott) G. Zhu. Croat 343 34.
Panama (MO); Dracunculus canariensis Kunth, Bogner
1519, Gran Canaria, a
Eminium alberti E Wills son & "ver 765, cult. (К);
E зг кыа 2402, Реги
Hotta, iiim cult. (M).

Gearum brasiliense М. E. Br., Burchell 8598, Brazil (К);
Gonatopus boivinii (Decne.) Engl., cult. (M); Gorgonidium
7 ‚ Bolivia, cult. (М); Gymnostachys anceps
6, Australia, cult. (M).

Hapaline brownii Hook.f., Burtt & куч 1771, cult.
(М); Helicodiceros muscivorus Engl., 1032/73, cult. (М);
Heteropsis spruceana 5 Schott, Croat 5 Panama (MQ);
Holochlamys beccarii Engl., Bogner 1269, New Guinea,
cult. (M); Homalomena peltata (Poepp.) Masters, Croat
38285, Canal Zone (M).

Jasarum ste кш Bunting, Herkner & Jeschke s.n.,
Venezuela, cult.

Lagenandra erosa DeWit, Bogner 450, Ceylon, cult.
(М); Lasia spinosa f. simplex Thwaites, Bogner 428, Thai—
ri cult. Lasimorpha senegalensis Schott. е

West Africa, cult. : D minor L., cult. (M):
ei camtschatcensis Schott, cult. (

Mangonia tweediana Se :hott, a 2376, Brazil, cult.
M: Monstera acuminata C. Koch, Croat 42933, Nicaragua
(MO); Montrichardia arborescens (L.) Schott, Croat 3833

Canal Zone (MQ).

Nephthytis afzelii Schott, Knecht 23/198, Cote d'Ivoire.
"TN (M).

Orontium aquaticum L.,
lina (МО).

Pedicellarum paiei M. ve Paie 16354, Sarawak,
cult. (K); Peltandra 19 (Michx.) Morong, Boufford
18467, E a (MO); Philodendron Wap ur imd Schott,
Ране bor neense M age
nellia tripartita 5с (wt
M) [хыз e elongata N, E: Br, ^
1478, Sarawak, cult. (M); Piptospatha lucens (Bogner)
Bogner & A. Hay Bins nd studied as Hottarum lucens],
Bogner 1439, Sarawak, cult. (M): Pistia stratiotes L., cult.
(MO); Podolasia stipitate nderson 26757, Sa-
rawak (K);
cult. (M); е Mu. (da Hook.,
sanayake 1016, rotarum sechellarum
Gardiner 110, Ce ce ine (К a Psendodracontium s siam
Gagnep., Kew 414—35—41401, cult. (M); Pseudohydrosme
gabunensis Engl., Breteler s.n., Gabon, qe (L ); Pycnos-
patha arietina Gagnep., Bogner 395, Thailand, cult. (M).

urabile Scl

Boufford 18027, North Caro-

Annals of the
Missouri Botanical Garden

Remusatia 1 (Roxb.) Se sag & Endl., spirit col-
lection (K); Rhaphidophora afric N.

602, Gabon, cult R
3792, Mexico ( h
Sauromatum guttatum Schott (= Typhonium), Keating
s.n., cult. Edwardsville, IL; Sc к gracilis Brongn.
ex Schott, Bogner 1211, a cult. (М); Schismatoglottis
calyptrata (Roxb.) Zoll. Mo pes MO hort.
112049, cult. (MO); Senda scortechinii Hook. f., Koer-
per s.n., Borne 0. cult. (M): Spathantheum orbignyanum

Schott, Rauh 26024, Pe ти, ШЕ ; Spathicarpa sagitti-
Pee Schott, Bogner 2335, cult. (М); Spathiphyllum fried-
richsthalii Schott, Croat 3212 Canal Zone (MO);
polyrhiza (L.) Sehleid., cult. (M)
angustifolium Hemsl., Croat 35255, Costa Rica (M

Steudnera M ud C. Koch, cult. (M); Styloc gn
crassispathus Bogner, Bogner 143, Tanzania, cult. (М);
Symplocarpus pus dus (L.) ‚ Keating 2275, Illinois;
Synandrospadix (Griseb.) Engl.,

1а „ Bogner
корша ip Schott,
Croat

accession

Spiro-

dela St 5

vermitoxicus Bogner

1480, M cult. (M); Syngonium angustatum Schott,
Croat 4 )).

а
—
me
=
©
=
2 oi
EE
@
7;
T

um dina ex Schott, н D
; Therio phonum mur nur oe Mooney 3

‚ Hay vgn
Rosner s.n., cult.

5 5 Schott. ‚ 401/75 cult. (М); Typhonodo.
num Schott, cult.

1 с atum E ме Jangoux et al. 85-058 21-
жашчы dinis Schott, ш 35706

ca
olffia кыа (L.) Horkel ex Wimm., cult. (M); Wolf-

fiella yee hii (Hegelm.) Monod, б. Egge rs s.n., Vene-
zuela, cult. (M

К шк sagittifolium (L.) Schott, Metcalfe s.n., Ca-
nal Zone (K).

Zamioculcas zamiifolia Engl., Bogner 126, Tanzania,

ilt. ); еей albomaculata (Hook. f.) Baill.,
Dur (MO); Zomicarpa riedeliana Schott, Bogner s
cult. (M); abans amazonica eit
Brazil, cult. (MO).

Croat

THE PHYLOGENY OF THE
COCOEAE (ARECACEAE)
WITH EMPHASIS ON
COCOS NUCIFERA'

Bee F. Gunn?

ABSTRACT

The t

ciosa, and Bactris gasipaes. This study, ba: sed on the

ribe Cocoeae contains. economically important RS including Cocos be у Elaeis guineensis, Attalea spe-
h

iclear prk gene sequence, addresses the monophyly of the

subtribes of Cocoeae, the closest re e of Cocos nuc ifera. and tikes nus sal ations of its distribution. The

Cocoeae are divided into the spiny and non-spiny taxa. Molecular data alone sugges
mly extant member of its
re and India were used as calibration points to estimate times of diver

the Cocos clade based on the phylogeny was postulated. It is кро that (
Africa, Madagascar, and India, and southward to Australia and New
The ania divergence dates were corroborated with major tectonic events

originate in the western Pacific; it may be the «

rb erica, diversified and radiated eastward te
уо via the Antarctic corridor.
Key words:

that Cocos nucifera did not
L ineage. Seve al Cocoeae fossils from New
ence of clades. A hypothesis for the origin
осоеае originated from South

\re ^caceae, C ocoeae, coconut, Cocos, prk gene.

Palms (Palmae or Arecaceae) have been impor-
tant in the lives of people since early civilization.

1972: 417) noted, palms provide “a

As Purseglove
wider range of economic products and multiplicity
of uses than any other useful plants: in economic
importance they are second only to the Grami-

Lr]

neae.” With the early domestication of the coconut,
palms played a vital role in the colonization of the
Pacific by the Austronesians (Bellwood, 1975).
The palm family includes 189 genera and about
2600 species found mainly in the tropics or sub-
tropics (Uhl & Dransfield, 1999),
They are especially di-

but sometimes in

—

warm temperate regions.
verse in Malesia and Amazonia, but are poorly rep-
resented in Africa (Moore, 1973a; Uhl € Drans-
field, 1987). Work on the phylogeny of angiosperms
has confirmed the monophyly of the palm family

and its position among the basal commelinids
(APG, 1998; Soltis et al., 2000).

Moore (1973a) arranged palms into 15 unranked
major groups based on the presumed order of spe-
cialization from a series of morphological charac-
ters. He recognized the cocosoid palms as a single
group because of their distinctive bony endocarps
with three pores, and he also recognized three sub-
groups within the cocosoids, the Bactris, Cocos, and

1987) later
Are-

caceae. Cocoeae were treated as a distinctive tribe

—

Elaeis alliances. Uhl and Dransfield

recognized six subfamilies and 14 tribes in

consisting of 22 genera divided into five subtribes
similar to Moore’s cocosoid major group but includ-
ing Beccariophoenix. The Calamoideae (100% bs)
and Phytelephantoideae (97% bs) are monophyletic
based on 18S molecular data, but the Coryphoi-
Ceroxyloideae, and Arecoideae are not (As-
2000; Hahn, 2002a); Nypoideae are

monotypic. The Cococeae are one of the eight tribes

deae,

mussen et al.,

of Arecoideae, and are divided into five subtribes,
20 genera, and 206 species (Table 1; Uhl &
Dransfield, 1987; Henderson et al., 1995).

Cocoeae contain several economically important
plants, including Cocos nucifera, Elaeis guineensis
(African oil palm), Attalea speciosa (babagu palm).
and Bactris gasipaes (peach palm). Despite their
economic importance, the phylogenetic history of
the tribe has not been studied, and we do not know
the closest relative of the coconut.

Nevertheless, the monophyly of Cocoeae is not
in doubt (Asmussen et al., 2000; Lewis & Doyle.
2001; Hahn, 2002a, b). А striking synapomorphy
of the group is the presence of three or more "eyes
or germination pores on the hardened seed endo-

I This research represents part of the work for a master's thesis from the d вну of Missouri-St. Louis, | thank

the following persons and institutions for their
University af Louis:
thanked for fresh or dried herbarium specime
of Forestry, West
Foundation, and N
? Appliec iind +h Dept.
bee.gunn@mobot.org.

Missouri-St.

SF-Deep Time Project travel gr

ANN. Missouni Bor.

generous aid and fin:
і

Р. М. онаа (МО)
Indie S. Funding was obtaine a I the International Center for Tropical Ecology. Ё

Missouri. Botanical pe»

ancial suppo : Р, К. Stevens and E. A. Kellogg.
A. J. Henderson (NY). The following institutions are
: FTG, K, MBC, MO, NY, and Saint Lucia Minis

. Desmond » ее
Missouri 63166-0299, U.S.A.

Louis,

P.O. Box 299,

GARD. 91: 505-522. 2004.

506 Annals of the
Missouri Botanical Garden
Table 1. Taxonomic hierarchy of tribe Cocoeae, sensu Syagrus are smaller and contain much less liquid
Uhl and Dransfield (1987) and Henderson et al. (1995). endosperm than those of Cocos nucifera.

Numbers of species are Poi by the taxon's distribu-
25).

tion (Henderson et al.

Subfamily: Arecoideae
ribe: Cocoeae
Subtribe: Attaleinae Drude
Attalea Kunth Neotropics)
Subtribe: Butiin
Allagoptera TER (4, South Americ
utia (Becc.) Becc. (7, South Amare :a)
Cocos L. (1, pantropical)
Jubaea Kunth n : hile
; South Africa)

e Saakov

—

Voanioala J. Dransf. (1, Madagascar)
Subtribe: Bactridinae
Acrocomia Ma it- (2; Neotropic 8)

©
а Рә;
=
BS

| у. (18, Neotropics)
Bactris Jacq. ex Scop. (73, South America)
Desmoncus Mart. (7, Neotropics)
Gastrococos Morales (1, Cuba)

Subtribe: Beccariophoenicinae J. Dransf. & Uhl
Beccariophoenix Jum. & H. Perrier (1, Mada-

gascar

—

Subtribe: merges iru
Elaeis Jacq. (2, . Neotropics)
Barcella Drude (. South America)

carp. Other distinguishing features include a once-
branched (rarely spicate) inflorescence, an incon-
spicuous prophyll, a prominent and often woody
peduncular bract that splits abaxially with respect
to the main axis of the palm, imbricate petals of
pistillate flowers, and a triovulate gynoecium (Uhl
& Dransfield, 1987).

Cocoeae are widely distributed in the Neotropics
(15 genera, Henderson et al., 1995), and two genera
are found in Madagascar (Beccariophoenix and
Voanioala) and two in Africa (Jubaeopsis and
Elaeis, the latter also found in South America),
while Cocos nucifera is pantropical. Historically, at
least 60 species were included in Cocos by Martius
(1824), Вессаг (1916), Barbosa Rodrigues (1903),
and Glassman (1987); these are now placed in ei-
ther Syagrus or Butia. Cocos and Syagrus share
many similarities, but may be distinguished by the
size of their flowers and their fruits. Syagrus has
globose pistillate flowers, and the apices of the se-
pals and petals are valvate. In contrast, Cocos has
globose-ovoid pistillate flowers, and the apices of

the sepals and petals are rounded. The fruits of

The fr

common in palms. Its epicarp is composed of scle-

uit of Cocoeae is a modified drupe, as is

renchyma, which contains raphides and secondary
compounds such as tannin. The mesocarp consists
mainly of parenchyma and is usually fleshy and
nutritious, for example, Syagrus romanzoffiana. In
Cocoeae, the parenchymatous mesocarp layer is
highly developed, and in Cocos it is thick and fi-
brous and contributes to buoyancy. The fruit en-
docarp is usually sclerenc -hymatous and is pre-
sumed 1o protect the developing seed from
predation, desiccation, or crushing (Essig, 1977).
Maturation of the fruit occurs basipetally in the Co-
coeae and Arecoideae (Uhl & Moore, 1971); this is
due to a basal meristemic zone that continues to
divide until the fruit reaches half its final length,
with further increase in fruit size due to cell en-
largement (Murray, 1973). Sclerification of the cells
also occurs basipetally; thus, the stylar regions be-
come hard and protective before the base of the
ovary (Uhl & Moore, 1971)

The current phylogeny of the Cocoeae suggests
hypotheses about the origin of Cocos nucifera,
which may have reached its present distribution by
water and/or human dispersal. Various authors have
suggested an origin in the western Pacific (Harries,
1978), Asia or Polynesia (Beccari, 1963; Corner,
1966), Melanesia (Moore, 1973b), or the Neotropics
(Guppy, 1906; Cook, 1910; Hahn, 2002b). Cur-
rently, it is accepted by most scientists that the
coconut probably originated in the western Pacific
(Harries, 1978; Gruezo & Harries, 1984).

Molecular studies in the Arecaceae are fairly
limited. Although family-wide studies conducted by
Asmussen et al. (2000) investigated relationships
among 65 species, only three representatives of Co-
coeae were sequenced from plastid genes, rps
intron and trnL-trnF. Baker et al. (2000) uae
22 genera, all from subfamily Calamoideae us
nrDNA (ITs) and cpDNA (rps16). Hahn (2002a)
conducted combined analyses of all available palm
data (65 species) including atpB, rbcL, 18S nr
DNA, and morphology. He reported incongruence

*

between the morphological and all the molecular
data sets and also general lack of resolution and
support. However, he noted the monophyly of Co—
coeae (86%) represented by two taxa, Beccario-
phoenix and Elaeis. Lewis and Doyle (2002) ex-
amined 54 palm species using nr malate synthase
and phosphoribulokinase (prk) genes for the Areceae
tribe; two Cocoeae taxa were included as outgroups.
Hahns (2002b)

sampled 51 representatives of the arecoid line and

Arecoideae phylogenetic study

Volume 91, Number 3
2004

Gunn 507
Phylogeny of Cocoeae

included 16 genera of Cocoeae using plastid genes
atpB, rbcL, and trnL-trnF. This present study is the
first comprehensive molecular investigation based
on the nuclear gene prk of all 20 extant genera in
Cocoeae. and 34 taxa were sampled across all five
subtribes.

The aims of this study are to test the monophyly

of Cocoeae subtribes Bactridinae, Butiinae. and

Elaeidinae, and to investigate the relationship of

Cocos nucifera within the tribe. A generic-level
phylogeny of Cocoeae is presented here. based on
the nuclear gene prk. A well-documented assem-
blage of Cocoeae fossil pollen and fruits from Af-
rica, Australia, Easter Island, France, Germany, In-
dia, New Zealand, and South America has been
compiled: several of the fruits were used to cali-
brate the divergence times of the clades.

MATERIALS AND METHODS
TAXA

Thirty-four taxa representing all 20 genera rec-
ognized for the five subtribes of Cocoeae were sam-
pled from living collections (33 accessions) and one
from a dried herbarium specimen of Parajubaea
torallyi (see Appendix 1). The sequences for the
two outgroups, Reinhardtia gracilis and Roystonea
regia, as well as that of one ingroup, Allagoptera
arenaria, were retrieved from GenBank. The out-
groups were chosen from results of the phylogeny
of the Arecaceae (Hahn, 2002a, 2002b) and of the
ewis & Doyle, 2002). Multiple acces-

sions of Cocos nucifera—two tall varieties and one

Arecoideae (

dwarf variety—were sampled, as they represented
two distinct domesticated forms of the coconut. Two
accessions of Aiphanes aculeata were sequenced
because Aiphanes caryotifolia 1s now synonymous
with Aiphanes aculeata (Borchenius & Bernal,
1996). Clones of the 34 taxa sequenced were in-
cluded in the MP analysis to verify that they were
all paralogue 2 of the prk gene (Lewis & Doyle,
2002)

DNA EXTRACTION

Genomic DNA was extracted from fresh leaves,
silica-dried material, or herbarium specimens using
large-scale CTAB and cesium chloride purifications
(modified from Doyle & Doyle, 1987) and miniprep
protocols (Doyle & Doyle, 1987). Phosphoribulok-
inase is an enzyme unique to the photosynthetic
carbon reduction cycle and catalyzes the irrevers-
ible ATP-dependent synthesis of ribulose-1, 5 bis-
phosphate. The coding sequence of the prk gene is
interrupted by four introns (Lloyd et al., 1991). This

low-copy nuclear gene has been found to be useful
in molecular studies at species and generic levels
(Lewis & Doyle, 2002). Sequences of about 700 bp
from exons 4, 5 flanking the fourth intron were ob-
tained,

PCR, CLONING, AND SEQUENCING

Double-stranded DNA was amplified using the
polymerase chain reaction (PCR). A two-step am-
plification protocol with semi-nested primers (488f
and 1167r from flowering plants (non-palms); and
717f and 969r from palms) was used. Primers for
the prk nuclear gene were designed by Lewis and
Doyle (2002). Máügic buffer (modified from drei
1990, with addition of DMSO) was used in the
cocktail.
PCR served as the template for the second step

Two pl of the product from the first 11

PCR (50 pl reactions) using the internal set of
primers designed for palms (717f and 969r: Lewis
& Doyle, 2001). Thermal cycling conditions were
as follows: 94°C, 4 min.,

94°C, 53°C, 1 min., 72°C, 2 min..
ing with 72°C, 7 min. PCR products were resolved

followed by 35 cycles at
| min., conclud-
on a 1% agarose gel, then purified by spinning
them through Qiaquik columns (Qiagen™). The
eluted products were further gel purified and
passed again through Qiaquik columns. Amplified
fragments of prk were then cloned using pGEM-T
easy vector systems (Promega Corp.), reamplified
with MI3R and MI3F (Kobs, 1995) universal prim-
ers, then purified with Qiaquik columns and re-
solved again on 1% agarose gels. Purified products
were cycle sequenced using Big Dye Terminator
(Perkin Elmer) using T7 and SP6 primers (Promega
Corp., 1996). For Bactris, Jubaeopsis, and one sam-
ple of Cocos nucifera the amplification primers 717f
and 969r (Lewis & Doyle, 2002) were used. The
sequences were generated on an ABI 377 auto-
mated sequencer at the University of Missouri-St.
Louis. At least three clones per plate were picked
from each taxon for sequencing. Both the forward
and reverse strands had overlaps of at least 70%,
although the Desmoncus chinantlensis sequence had
less overlap (60%). Contigs were assembled using

Sequencher™ 3.1 (Gene Codes Corporation, 1991—
1998)

SEQUENCE ALIGNMENT

Preliminary global alignments were performed
using CLUSTAL X, Ver.1.8, 1999 (Thompson et al.,
1997) and realigned visually with SE-AL
1.dl (Rambaut, 1996). Sequences of each clone, in-

version

cluding some direct sequences, were used for each
individual taxon in the phylogenetic analysis (Fig.

508

Annals of the
Missouri Botanical Garden

1). Sequences were deposited in GenBank (acces-
sions AY601206—AY 601273)
PHYLOGENETIC ANALYSIS

Parsimony analyses of molecular data were con-
ducted using PAUP* 4.0b10 (Swofford, 1999).
Maximum parsimony analyses (MP) were performed
with heuristic search options as follows: tree-bisec-
tion-reconstruction (TBR) branch swapping, gaps
coded as missing. The first 20 and last 24 char-
acters were excluded from the analysis because
they were the primer sites. Also excluded was the
poly-A and С region in the fourth intron (bp 370—
385) because it could not be unambiguously
aligned. All characters were unordered, equally
weighted, and outgroups were specified. Internal
support for the clades was assessed by bootstrap-
ping, with 100 replicates with 1000 random taxon
addition replicates and TBR swapping.

Maximum Likelihood (ML) analyses were carried
out using PAUP* 4.0b10. MODELTEST 3.06 (Po-
sada & Crandall, 1998) was used to obtain the sub-
stitution model that fits the data best. MODELTEST
3.06 uses PAUP* to calculate likelihood scores for
56 models of evolution and compares the different
nested models. Settings from the model test were
used in PAUP to generate the maximum-likelihood
tree using the Hasegawa-Kishino- Yano iu or

G model, with base frequencies: A
0.2948, С 0.1990, C = 0.2256, Т = 0.2806;
transition/transversion ratio = 1.8755; and gamma
1.0177.

heuristic search strategy with 100 random taxon ad-

distribution shape = ML searches used a
ditions, holding five trees per step, TBR (tree bi-
section reconstruction), and branch swapping. The
ML analyses were performed with and without mo-
lecular clock constraints. Under the clock regime,
the maximum likelihood analysis was stopped after
the log likelihood value reached a maximum like-
lihood of 4052.0311 and remained unchanged for
two hours afterward.

The likelihood ratio test based on the differences
between the log-likelihood of the two models indi-
cates that the molecular clock could be rejected
(**P < 0.01, df = 38). In order to infer age of
divergence of the clades (in ML tree, Fig. 2), a Non
Parametric Rate Smoothing (NPRS) of the tree was
applied using the r8s program (Sanderson, 2000).
Four fossils were used to calibrate the internal
nodes of the tree. The fossils (see Fig. 2) F1 (Whar-
ekuri—32 my), F2 (Boulder Hill, NZ—42 my), F3

(Waihao beaked—31 my), and F4 (Cocos intertrap-

peansis, India—50 my) were used separately to cal-

ibrate the internal nodes. The long branches of

Reinhardtia, Roystonea, and Barcella were pruned
because the rapid change of substitution rates from
the long to short branches affected the estimated
ages of divergence. A penalized likelihood analysis
was used, which finds an optimal smoothing param-
eter or autocorrection to ameliorate the effects of
rapid changes on tree and pruning. The estimated
rates of divergence based on the chronograms (not
shown) are included in Table 2

Bayesian inference of phylogeny is a statistical
approach based on the likelihood function and the
prior probability distribution of trees (Huelsenbeck
2002). The MrBayes (Huelsenbeck, 2000)
program uses the Metropolis-coupled Markov Chain

et al.,

Monte Carlo to sample the best trees from the dis-
tribution of the posterior probabilities. The same
Nexus data file created in PAUP was used in
MrBayes 2.01 to generate the tree with the posterior
The MODELTEST 3.06

parameters used for the ML analysis were

probability closest to
model
also used in the Bayesian analysis. ‘Two million re-
arrangements were run, and every 1000th tree was
saved. The burn-in number of trees was 1600.

RESULTS

The total length of the prk aligned sequence was
672 nucleotide substitution sites. The maximum
pairwise distance between sequences was 16%
among the taxa excluding the outgroup. Pairwise
similarity of the clones within a species was 93%-—
99%. The PCR error was 0.03%.

The MP topology for Cocoeae with all the clones
included (72 sequences) shows the monophyly of
the cloned taxa (Fig. 1). In the strict consensus of
14.071 MP trees, tree length was 524, the consis-
tency index (СІ), excluding uninformative charac-
ters, was 0.733, rescaled consistency index (RC)
was 0.668, and the retention index (RI) was 0.911.
The division of Cocoeae (excepting Barcella) into
two main clades (Fig. 1), the non-spiny (94% boot-
strap support (bs)) and spiny (98% bs) species, is
fairly robust in this topology. Barcella odora is Бае
al in Cocoeae (55%), with the clade forming the
rest of the tribe having 78% bootstrap support. The
non-spiny group includes a large clade (94% bs),
plus Beccariophoenix madagascariensis and Voan-
iaola gerardii in a basal position (57%). Within the
large non-spiny clade are the Cocos and Attalea
The

Cocos alliance itself (5396 support) is composed of

alliances with Jubaeopsis caffra unresolved.
Cocos nucifera, (Allagoptera leucocalyx + Polyan-
drococos caudescens), (Butia capitata, eriospatha +
Jubaea chilensis), (Syagrus атага + S. smithii,
100% bs) with Parajubaea torallyi unplaced. Butia

Volume 91, Number 3
2004

Gunn
Phylogeny of Cocoeae

100

Aiphanes minima

Aiphanes aculeata Clone A2
Aiphanes aculeata Clone A3
Aiphanes aculeata

| Aiphanes aculeata Clone Al
| 52 ا‎

89

SPINY

83 [ — Acrocomia aculeata
| Gastrococos crispa Clone Al
strococos crispa

p

Elaeis guineensis Clone A1

раш guineensis Clone А2

Cocos nucifera
Cocos nucifera

a

*

al Clone B2
4 pcos nucifera

tall) Clone C1
‹

Butia а
ilensis

COCOS ALLIANCE

gagis amara Clone A

Syagrus smithii Clone 45

Syagrus smithit С
agrus smithii Clone A3

| 00 nont
a
Syagrus smithii Clone A4

—. p —— Рағајиђаеа torallyi Clone Al

— ——— Parajubaea torallyi Clone A2

era

Attalea phalerata Clone A
Attalea счабегазд а Clone А
Attalea speciosa Clone A1

Attalea speciosa Clone
yagrus eon ana
'vagrus romanzó]ftana

A2
Лопе Al

94

Lytocaryum wed
ocary

NON-SPINY

— ͤ Т
—

е
Jubaeopsis caffra Clone Al
Jubaeopsis caffra Clone A2
Beccarioph. madagascar. Clone Al
Be ph. ma h

ATTALEA ALLIANCE

‘carioph. madagascar. Clone A2
сс сы UY fe. " 2

Г Beccarioph. madagascar.

Voanioala gerar

ке capace

ii
Voanioala gerardii Clone Al
oanioala gerardii Clone A2
/oanioala gerardii Clone АЗ

ata

}
|

__ pM
|

Voanioala gerardii Clone A4
Voanioala gerardii Clone A5
Barcella odora Clone Al

р
| Barcella сап Clone A2

arcella odora

Reinhardtia gracilis

Figure

Maximum parsimony tree including clones. Strict consensus of 14,071 trees; tree len

Roystonea regia

th = 524; CI =

0.733; RC = 0.668; RI = 0.911. Percentages above branches show bootstrap values. The abbreviation Beccartoph.

madagascr. = Beccariophoenix madagascariensis.

capitata is closely related to B. eriospatha (95%
bs), both forming a well-supported sister group to
Jubaea chilensis (99% bs). Polyandrococos caudes-
cens is nested within the clade composed of Alla-
goptera leucocalyx and A. arenaria (92% bs). The

Attalea alliance (79% bs) comprises the Attalea
clade (100% bs) and its sister group, (Syagrus ro-
manzoffinana + Lytocaryum weddellianum, 100%
8

ы

The spiny palms include Elaeis (2 species), Ac-

Annals

510 of the
Missouri Botanical Garden

Table 2. Estimated divergence times of clades. N = node; F1 = Boulder Hill, New Zealand (42 mya), F2 = Cocos
intertrappeansis, India (50 mya), Cocoeae fossils for setting minimum age constraints. Columns 1, 2, 3, and 4 represent
¿ocos nuccifera + E + Polyandrococos)
+ (Syagrus roman-

=

the estimated times of divergence of the clades. и alliance = (

rus amara + 3. sm

+ (Butia + Jubaea) + (Syagr hit) + Parajubaea). Attalea alliance = (Attal

zoffiana + Lytocaryum weddellianum)). DRE Reinhardtia gracilis and Rovstonea regia.

Chronograms/mya 1

Outgroups: Reinhardtia and Roystonea —
Cocoeae:

| divergence 60.45(N 1)

Sui cla 42(F 1
Malagasy clade 12.06(N26
5 e 35.72(N50
iocos alliance 37.04(N27
Ыш. а allianc 'e 34 87(N51

Parajubaea torallyi
Cocos nucifera
Elaeis guineensis + E. oleifera

51.02(N25)

2 3 4
56.12(N1) 96.61(N1) 15.31 (N1)
53.26(N2) 61.09(N2) 60.7 1(N2)

50(F2) 50(F2) 50(F2)
43.07(N4) 42.88(N5) 42.93(N6)
46.29(N43) 46.28(N44) 46.28(N45)
39.64(N5) 39.42(N6) 39.48(N7)
37.84(N6) 37.62(N7) 37.68(N8)

34.16(N 19) 33.96(N20) 34.01(N21)
37.84(N6) 37.62(N7) x ~
29.62(N21) 29.44(N22) 48(N2
26.84(N22) 26.67(N23) TIN E
2(F I 2(F 1) 42(F1)

—

Comparisons of estimated times of divergences of clac
different fossil calibration points.

rocomia (2) plus Gastrococos, Bactris plus Astrocar-
yum (2). Desmoncus, and Aiphanes.
phyletic (100% bs; E. guineensis +E. oleifera) and
is sister to the rest of the spiny group (100%). Ac-
rocomia (8196 bs) is paraphyletic, with Gastrococos
crispa forming a clade with Acrocomia aculeata
(83% bs). Species of Astrocaryum and Bactris form
a clade (76% bs). The three species of Aiphanes
form a monophyletic group (100% bs). The position
of Desmonc us chinantlensis is unresolved.

The ML tree (Fig. 2) had a -In = 3824.8914.
From the MODELTEST 3.06, HKY + G model was
selected as the best model of substitution. Base fre-
quencies used were: freq. A = 0.2948, freq. C =
0.1990, freq. G = 0.2256, and freq. T = 0.2806.
The Ti/tv ratio was 1.8755 and the gamma distri-
bution shape was 1.0177. MODELTEST
culates the Aikaike Information Criterion (AIC),
which compares unnested models of evolution. The

TVM+G and the AIC

Elaeis is mono-

—

also cal-

model selected was was
7670.2085.

The ML (Fig. 2) and Bayesian (Fig. 3) analyses
recovered trees that were consistent with the MP
topology. They also show Cocoeae separated into
non-spiny and spiny clades (100% prior probabil-
ity), and the taxa have the same relative positions
as in the MP tree.

Barcella is basal in Cocoeae,
long branch (0.117 substitution/site): its basal po-
sition is well supported in the Bayesian topology
(94% posterior probability). The two Malagasy Co-
coeae, Beccariophoenix and Voanioala, are basal
and sister to the non-spiny group (99% posterior

but is on a very

s from chronograms (not shown)

l and 2, 3, and 4 using

probabilty (pp)) in both topologies MP and Bayes-
ian. Jubaeopsis appears to be sister to the Attalea
alliance clade in the ML topology with no signif-
icant support, but is only weakly supported in the
Bayesian analysis. Attalea is monophyletic (100%
pp) and is sister to Syagrus romanzoffiana plus
Lytocaryum weddellianum (100% pp), as also in
the ML tree. The branches separating most taxa
within the Cocos alliance are short, and this lack
of resolution is also reflected in the Bayesian anal-
ysis. The basal branch (0.003 substitution/site)
within this clade is formed by (Syagrus smithii +
5. amara). There is robust support for the sister
relationship of this clade (100% pp). Relation-
ships among the three taxa Allagoptera arenaria,
A. leucocalyx, and Polyandrococos caudescens are
fairly well supported (0.006 subs./site) as in the
MP (92% bs) and Bayesian (100% pp) topologies.
Jubaea chilensis was sister to Butia eriospatha and
В. capitata, and this clade is also well supported
in both the MP (99% bs) and Bayesian trees
100% pp). Cocos and Parajubaea are joined on a
very short branch (0.001 subs./site). Parajubaea
is on a branch with 0.023 subs./site and in a clade
with Cocos nucifera (0.035 subs./site); in both MP
and Bayesian analysis (100% bs, pp) the dwarf
form is also basal.

The two Elaeis species form a monophyletic
group (0.037 subs./site; 100% posterior probability)
and are basal in this clade as also observed in the
MP analysis. The monophyly of Bactridinae (Acro-
Aiplanes, Astrocaryum, Bactris, Desmoncus,

Table

—

comia,

Gastrococos, is again indicated (0.016

Volume 91, Number 3 Gunn 511
2004 Phylogeny of Cocoeae

0.003. UN
Fl 0.034 Ше тїпїта
0.002 poe aculeata
003 Aiphanes caryotifolia

0.002 0.007
Acrocomia media
F2 ,
^w. 0.002 Acrocomia aculeata
. NEO
0.016 ).006 ! Gastrococos crispa
Bactris maraja
Astrocaryum gynacanthum
Astrocaryum paramaca
22 Desmoncus chinantlensis
* ; Áp
0.037 E Elaeis oleifera
0107 деу guineensis AFR |
0.003 S у
0.008 P» VAgQFUS smithii
0 Вуавт us атага МЕО
Parajubaea torallyi
0.901 0.002. |
` Cocos nucifera (dwarf)
А 0.009 ,.. p
F4 0.007 | 0.002 Cocos nucifera (tall)
0,002 З T PAN
1 Cocos nucifera (tall)
0.011 { . Й
Butia capitata
00 —
Butia eriospatha
0.016 |
Jubaea chilensis
0.011
0 Allagoptera leucocalyx
0.005 0. Polvandrococos caudescens
“Г 0.0
"^7 Allagoptera arenaria
е МЕО
Attalea oleifera
0.013 Attalea cohune
0.010 q ага phalerata
0.012 Attalea cuatrecasana
3 Attalea speciosa
OOD iio ane
0.002 Svagrus romanzoffiana
Lytocarvum weddellianium
Jubaeopsis caffra AFR |
0.013 Beccariophoenix madagascariensis
0.001 0010 , . "^
е Voanioala gerardii (Clone Al) MAD
0.00: Voanioala gerardii (Clone AS)
0.117 Barcella odora
0.033 Р Vs >]
Reinhardtia gracilis NEO
0.044

Rovstonea regia

———— 0.01 substitutions/site

AFR- Afr

MAD - сае
NEO - Neotropics

PAN - Pantropical

‘igure 2. d likelihood tree. Model used = HKY + G; base frequencies: A = 0.2948, C = 0.1990,
0.2256, T = 0.2806 . rsion ratio = 1.8755; gamma distribution shape = 1.0177; Aikaike ea
Criteria (AIC) = Ka 0.2085. Values above branches show number of nucleotide substitutions/site. F1, F2, and F3 =
Cocoeae fossils. = Whare 9 New Zealand (32 mya). F2 = Boulder Hill, New Zealand (38—45 туа). ЕЗ = Waihao

beaked, New Ze v (27-31 mya). F4 = Cocos intertrappeansis, India (50 mya).

512

Annals of the
Missouri Botanical Garden

Roink Ati. 27:

Roystonea regia

100

100

100 Aiphanes minima
A phan aculeata

ip aryotifolia
Acrocomia media
Acrocomia aculeata

pa

Bactris maraja

SPINY

100 Astrocaryum gynacanthum
Astrocaryum paramaca
Е ,

"nj

100

[ —— Elaeis oleifera

100

— laeis guineensis
100 Syagrus smithii
Syagrus amara

Parajubaea torallyi

Cocos nucifera (dwarf)
Cocos nucifera (tall)

Cocos nucifera (tall)
Allagoptera leucocalyx
Polyandrococos caudescens

Allaeontera aren
Sul

100 Butia capitata
Butia eriospatha

Jubaea chilensis

NON-SPINY

Attalea oleifera
Attalea cohune

Attalea phalerata
Attalea cuatrecasana
Attalea speciosa
Syagrus romanzoffiana

Lytocaryum weddellianium

Jubaeopsis caffra
Beccar. madagascr.

Lp

Voanioala gerardii (a)

Voanioala gerardii (b)

ure 3. Bayesian Tree. Values above branches show

madagascr. — Beccariophoenix madagascariensis.

subs./site; 100% pp). There is, however, not much
further
branch leading to Acrocomia media and (Acrocomia
aculeata + Gastrococos) is relatively short (0.002
subs./site; 94% posterior probability). There is rea-
sonable support for an Acrocomia aculeata and
Gastrococos crispa clade (100% pp, Fig. 3). Bactris
maraja and Astrocaryum form a clade held by a
short branch (0.003 subs./site), but that is well sup-
ported in the Bayesian tree (9996 pp). Aiphanes
forms a monophyletic group (100% pp, Fig. 3) with

resolution within the Bactridinae. The

Barcella odora

percentages of prior probability. The abbreviation Beccar.

a branch length of 0.034 subs./site. In both the ML
and Bayesian analyses, Desmoncus chinantlensis is
unplac ‘ed within the Bactridinae.

ıe two oulgroups Reinhardtia and Roystonea
form the innermost node. The ML topology shows
good support for nodes in the deeper parts of the
tree, but weaker toward the terminals. In the Bayes-
ian and ML analyses, there was better resolution
within the Butiinae (sensu Uhl & Dransfield, 1987),
showing a Cocos alliance (93% pp) and an Attalea
alone 'e (100% pp).

a

Volume 91, Number 3
2004

513
Phylogeny of Cocoeae

DISCUSSION

The MP, ML, and Bayesian topologies support
division of Cocoeae into two major clades, generally
corresponding to spiny and non-spiny taxa. Indeed,
Martius (1850:
277-304) for these groups to classify the Cocoinae

the presence of spines was used by

into his (i) Genera aculeata” [with spines] and ii)
Genera inermia” [without spines].
Bactris and other members of the spiny clade are
emergences from the epidermis of the whole palm.
However, Elaeis guineensis and E. oleifera, basal in
the spiny clade, have both fiber spines coming from
the midribs of the lower pinnae of the leaf, and
inflorescence spines, which are modified rachillae
1963). The non-spiny clade in-

cludes Butia and Syagrus, which may have petiolar

tips (Tomlinson,

spines, modified from leaf sheath fibers (Tomlinson,
1963). Spines appear to be homoplasious in Co-
coeae.

Barcella odora appears to be basal in the Co-
coeae and is sister to both the spiny and non-spiny
cocosoid palms (Figs. 1, 3). Barcella is monotypic
and is found only in the Amazon region in Brazil
north of the Rio Negro growing on white-sand soils
in Brazil. James Trail first described the palm in
1874

from Elaeis by its lack of petiole spines and

as Elaeis (subg. Barcella Trail), but it differs

inflorescence borne on a long peduncle. The inflo-
rescence is made up of either all staminate or both
staminate and pistillate flowers, but an Elaeis inflo-
rescence bears either staminate or entirely pistillate
flowers. These differences led Drude to recognize
Barcella as a distinct genus in the Palmae for Flora
1986). like

Elaeis, its flowers are large and are sunken in pits

Brasiliensis (Henderson, However,
on the rachillae, whose tips may form sharp points.
Barcella has been traditionally placed within sub-
tribe Elaeidinae together with Elaeis guineensis and
E. oleifera (Uhl & Dransfield, 1987). A Templeton
(Wilcoxon signed-ranked) test showed that there
was no significant difference between the two MP
topologies when Barcella was гае into а
clade with Elaeis (Р > 0.05, п =
that Elaeidinae may not be polyphyletic and that

17). This suggests

Barcella may be a member of the spiny clade, its
a

my

rachillae tips being the modified “spines
would then characterize this subtribe.
Chromosome studies of the spiny clade show that

(Read, 1966:
Röser, 1999) except for Elaeis, which has л = 16.

they have a haploid number of 15

On the other hand, all members of the non-spiny
clade have n = 16 pd for Beccariophoenix mad-
agascariensis (n 18), perhaps Jubaeopsis caffra

(n = 80-100)

Re a 1966). and Voanioala gerardii

The spines of

(п = 298) (Johnson et al., 1989), a probable auto-
polyploid. Voanioala is basal in the non-spiny Co-
coeae, and its chromosome number is the highest
recorded for monocotyledons. Voanioala gerardii is
a large, slow-growing palm restricted to Madagas-
car, suggesting that it is an evolutionary relict
which has undergone successive mitotic doublings
or selfing of unreduced gametes to form a repro-
ductively isolated high autopolyploid (Johnson et
al.. 1989). In the ML and Bayesian analyses for V.
gerardii, two divergent sequences were isolated
from the clones and in both topologies they show a
sister relationship to one another with good support
(97% pp. Fig. 3). In the MP topology they form a
basal trichotomy in the non-spiny clade with Bec-
cariophoenix.

Beccariophoenix madagascariensis plus Voanioa-
la gerardii are basal in the non-spiny clade. Like
Voanioala, Beccariophoenix is endemic to Mada-
gascar growing in the white-sand and submontane
A
the Areceae by Beccari and Pichi-Sermolli (1956)
and Moore (1973a), it was placed in the Cocoeae
by Uhl and Dransfield (1987), based on the syna-

pomorphies of its woody and beaked peduncular

rain forests. Formerly thought to be a member

bract and three endocarp pores. The inflorescences
are massive and torpedo-like borne on a long pe-
duncle. The fruit is single-seeded, purple-brown
with a thin but woody endocarp. In its root anatomy,
it has the same single-layered, unevenly thickened
tanniniferous exodermis as in Cocoeae (Seubert,

Jubaeopsis caffra has an unresolved position
within the Cocos and Attalea alliances: however, it
may be basal in the clades formed by these alli-
ances (57% bs: see Figs. 1, 2). Its morphology
closely resembles that of Jubaea and Butia, differ-
ing from Jubaea by its clustering habit, non-stalked
staminate flowers, and separate sepals and from
Butia in its many stamens (18) and lack of petiolar
spines. The three are similar in having lateral pores
on their endocarps, a rhizodermis with large un-
evenly thickened cells, and exodermis with tanni-
1998a).

endemic to East Pondo-

niferous, evenly thickened cells (Seubert,
Jubaeopsis is monotypic,
land, South Africa; it is also a polyploid (2n =
160—200: Read, 1966).

Lytocaryum weddellianum is closely related to
Syagrus romanzoffiana (100% bs, 100% pp, Figs.
1, 3) and forms a clade in the Attalea alliance.
Lytocaryum is restricted to southeastern Brazil and
is similar to Syagrus romanzoffiana in having en-
docarps with three internal shiny vertical lines and
basal pores, but differs in its thin endocarp. Al-
though there is good molecular and morphological

514

Annals of the
Missouri Botanical Garden

evidence for the synonymy of Lytocaryum with Sya-
grus (Henderson et al., 1995; cf. Figs. 1-3 herein),
the formal reduction of Lytocaryum is not proposed
here. Syagrus is a large complex genus of 30 spe-
cies and appears to be polyphyletic with 5, атага
+ S. smithii forming a clade in the Cocos alliance
and the type species, Syagrus cocoides, has nol
been sequenced.

The five species of Attalea studied form a mono-
phyletic group. Attalea is a large Neotropical genus
of 29 species that possess distinctive inflorescence
types, with individuals bearing either staminate or
androgynous flowers (Glassman, 1999). Previously
six genera, Attalea, Markleya, Maximiliana, Orbig-
Parascheelea, and Scheelea, were recognized
1999; Balick, 1991)

based on characters of the stamens and petals of

nya,

Glassman, Henderson. &

pm

the male flowers. Molecular evidence here shows
that these genera differ from each other by only one
Attalea (.I.) has a fairly ho-
mogeneous root anatomy (Seubert, 1998b) and pol-

or two bp positions.

len morphology (Thanikaimoni, 1971): this, togeth-
lac k of

morphological (Tomlinson.

other | distinguishing
1961) and :
ular characters, suggests that this group should be
Attalea.

The closest relative to Cocos nucifera is still un-

er with the
now molec-

united into one genus,

resolved, but this species probably belongs to the
clade referred to here as the Cocos alliance, com-
prising A//agoptera plus Polyandrococos, Butia plus
Jubaea, Syagrus smithii plus S. amara, and Para-
Jubaea. All these palms occupy habitats with low
rainfall and sandy soils. Allagoptera arenaria grows
in the restinga, and Polyandrococos caudescens is
found in open lowland areas within the Brazilian
1996; Hen-
in southern

Atlantic coastal forest (Lorenzi et al.,
1995).
subtropical South America and Jubaea is endemic

derson et al., Butia is found
to Chile. Parajubaea is found in Bolivia, Ecuador,
and southern Colombia. Syagrus amara is native to
the Lesser Antilles and found in coastal ravines,
while Syagrus smithii is found on lowland forest on
non-inundated soils in northwestern South Ameri-
ca. Cocos nucifera is a strand plant with wide dis-
tribution throughout the tropics.

The three sequences for Cocos nucifera were tak-
en from one dwarf and two tall forms of the coconut
1949).

vated from the Pacific and Melanesia (region oc-

(sensu Narayana & John, They were culti-

—

cupied by Melanesian people). They form a mono-
phyletic group (100% bs), but

moderately long branch (0.035

subtended by i

subs./site). Cocos
nucifera may perhaps be more closely related to
Parajubaea than to other members of the Cocos al-
liance. In the ML analysis, Parajubaea torallyi re-

solved as sister to Cocos nucifera, but on a very
short branch; two nucleotide bases are in common
between the two supporting this branch. Paraju-
baea torallyi grows naturally in the humid valleys
of sandstone mountains of the central and southern
Bolivian Andes at approximately 2000 m altitude
Uhl & Dransfield, 1987; Moraes, 1996). This Bo-
livian palm has been relatively unknown since its
original description by Martius (1847a, as Diploth-
emium). Since then it has been shifted to Jubaea
(Wendland, 1878), Allagoptera (Kuntze, 1891), and
Polyandrococos (Barbosa Rodrigues, 1901). Max
Burret (1930) proposed the name Parajubaea for

pamm,

this genus with P. cocoides, a cultivar found in Ec-
1990),
type. Parajubaea was placed in the Butiinae by Uhl
and Dransfield (1987
baea and Syagrus, and indeed, morphological dif-

uador (see Moraes & Henderson, as the

—

based on its similarity to Ju-

ferences between them are very slight. Parajubaea
has 13 to 18 stamens, whereas Jubaea has 18 and
Syagrus has 6. The endocarp of Parajubaea bears
ridges, while it is crested in Jubaea. Moraes and
Henderson (1990) also noted that the rachillae of
Parajubaea cocoides have small side branches, not
seen in the rest of the Butiinae (sensu Uhl & Drans-
field, 1987).
and the fruits of Parajubaea are dispersed by riv-

The mesocarp is fleshy and fibrous.

erine and animal means (Vargas, 1994),
Allagoptera is closely related to Polyandrococos
(92% bs, 100% pp, Figs. 1, 3). and both share the
synapomorphy of spicate inflorescences. Allagop-
tera includes four species, all acaulescent and with
dichotomous branching subterranean stems (Tom-
linson, 1967). The distinctive irregularly grouped
pinnae inserted at various angles characterize three
of the four species as well as Polyandrococos cau-
descens (Mart.) Barb. Rodr.

layer, and there is also a woolly tomentum. Waxy

The cuticle has a waxy

cuticles are also found in Syagrus атага (Jacq.)
Mart.

molecular as well as morphological evidence sug-

and Polyandrococos caudescens. The strong
gests that monotypic Polyandrococos caudescens be-
longs in Allagoptera.

Both morphological and molecular evidence sug-
gests the sister relationship of Butia and Jubaea
chilensis (see also Glassman, 1987; Uhl & Drans-
field, 1995). Butia differs
from Jubaea chilensis in having 6 instead of 18 sta-

1987; Henderson et al..

mens, unclustered pinnae, with usually oblique
split tips of the pinnae versus acuminate symmet-
rical tips, and in petiolar spines present versus

The fruits of Butia may be one- to three-

—

lone.
chambered, as in Butia capitata, but are usually
one-chambered in Jubaea. The Chilean wine palm,

Jubaea chilensis, is monotypic and endemic to

Volume 91, Number 3
2004

Phylogeny of Cocoeae

Chile. The close relationship between Butia and
Jubaea is further corroborated by similarities in
leaf (Glassman, 1987) and root anatomy (Seubert.
1998), possession of smooth or striate spathes, and
the embryo pores in the equatorial position on the
endocarp.

1995)

is predominantly a South American genus, with one

Syagrus (30 spp. sensu Henderson et al.,

species (S. amara) found in the Lesser Antilles. Ht
is most speciose in Brazil (22 spp.). where it is one
of the main plants of the cerrado and campo ru-
pestre. [ts taxonomie history has been closely
linked with Cocos, and taxa have been transferred
from Syagrus to Cocos. For example, Syagrus san-
cona Н. Karsten (1856) was shifted to Cocos san-
cona (H. Karsten) Hook. f. (1882) and back again
to Syagrus sancona (Н. Karsten) Hook. f. (Glass-
1979),
was transferred to Syagrus amara (Jacq.) Mart.

(1847b). to Rhyticocos (Jacq.) Bece. (1886), and to

Syagrus amara by Glassman (1970). Molecular ev-

жыды

man, Similarly, Cocos amara Jacq. (1705

idence (herein) suggests that Syagrus may be poly-
phyletic. However, Syagrus amara and 5. smithii
form a clade with strong support (100% bs and pp).
The fruits of these two Syagrus are elliptical with
prominently ridged endocarps with basal pores and
ruminate endosperm.

In the spiny group, subtribe Bactridinae is mono-
phyletic herein in all three topologies and includes
Aiphanes, Acrocomia, Gastrococos, Bactris, Astrocar-
yum, and Desmoncus. These Neotropical palms are
characterized by their emergent spines and fruits
with hardened endocarps.

Species of Aiphanes (22) are very spiny under-
story palms found predominantly in the Antilles
and western South America (Borchsenius & Bernal.
1996). The genus is monophyletic herein (100% bs,
Fig. 1). with several distinctive morphological char-
acters within Cocoeae: praemorse pinnae, staminate
and pistillate flowers with free sepals, and protan-
drous inflorescences.

Both species of Acrocomia and Gastrococos crispa
form a well-supported clade in the MP and Bayes-
ian trees (81% bs, 94% pp, Figs. 1. 2).

good indication that Acrocomia aculeata and Gas-

There is

trococos crispa are closely related (83% bs, 100%
pp. Figs. I. 3) differing by only two bp positions.
The genus Acrocomia is native from the West Indies
to southern Brazil, and was erected by Martius in
1824 for a single species (A. aculeata). Since then
25 species have been added, with Beccari (1912)
recognizing 15 species, but there has been no sub-
sequent systematic revision of this genus since Bai-
ley (1941).

tall palms with a crown of plumose-like pinnate

Species of Acrocomia are heavily armed,

leaves. They inhabit dry, non-inundated regions
with impoverished soils, and their fruits are com-
monly dispersed by cattle. Gastrococos crispa is
monotypic and endemic to Cuba and is vegetatively
similar to Acrocomia, the two differing mainly in

floral arrangement and morphology. The pollen of

the two genera are very similar, differing only in

1971).

Bactris currently contains some 73 species grow-

size (Thanikaimoni,

ing mostly in Central and South America (Hender-
son, 2000). In my analyis, it is sister to the Astro-

caryum clade (Astrocaryum paramaca + A.
gynacanthum), with which it ches several ilia
acteristics (76% bs, 99% pp. Figs.

distinguished by the lower surface a the pinna be-

‚ 3). И may be

ing pale gray-green not white tomentose as in As-
trocaryum. with the exception of Bactris bidentula
and B. glaucescens (Henderson, 2000).

All but one species of Desmoncus are armed with
climbing hooks and represent the New World eco-
logical equivalent of the rattans (Calamoideae, Are-

caceae), although there is no close phylogenetic re-

ationship between the two.

Elaeis has two closely related species (100% bs
and pp. Figs. I. 3), forming the basal clade in the
spiny cocosoid palms. Elaeis may be distinguished
by its unisexual inflorescences with flowers borne
in shallow pits on the spiny rachillae. Elaeis gui-
neensis. the economically important oil palm. and
Elaeis oleifera are interesting because they are the
Africa

These two taxa

only Cocoeae that are distributed both
and South America, respectively,
may represent the Gondwanan relationships of the
197

—
—

Cocoeae (see Thanikaimoni,
Times OF DIVERGENCE

The divergence times among the spiny cocosoid
palms were not easily discernible due to the poly-
tomy at the node subtending the Bactridinae. The
divergence time for the split of the spiny and the
non=spiny Cocoeae lineages was estimated to be
around 50-60 mya. The two Madagascan monotyp-
ic endemies, Beccariophoenix and Voanioala,
seemed to have diverged from the rest of the non-
spiny lineages about 40-51 mya. The Cocos alli-
ance group diversified from the Attalea alliance
group apparently about 40 mya. Cocos nucifera
seems to have diverged from its sister lineage Pa-
rajubaea about 22-27 mya. Jubaeopsis caffra, en-
demic to Pondoland, southeast Africa, diverged
from its sister lineage around 36—38 mya.
COCOEAE FOSSILS

The earliest unequivocal palm fossil record
from the Upper Cretaceous Magothy Formation of

516

Annals of the
Missouri Botanical Garden

Santonian (84 mya) (Daghlian, 1981). According to
Moore (1973b) and Raven and Axelrod (1974),
palms may have originated in West Gondwana—
Africa, South America, and part of Antarctica. Pal-
moxylon patagonicum was found in Chubut Prov-
ince, Argentina 1968). Сосоеае
trichotomosulcate pollen is observed frequently

(Romero,

only in Acrocomia, Gastrococos, and Elaeis (Thani-
komoni, 1971; M. Harley, pers. comm.). Pollen
characteristic of Acrocomia type 3 and known as
Trichotomosulcites antiquus was reported from the
Maastrichtian (65 mya) of Germany by Krutzsch
and Lenk (1969), They described it as having a
reticulate exine and a clearly differentiated simple
tectate margin next to the aperture. Although Ac-
rocomia has trichomosulcate pollen, it has coarsely
perforated exine; on the other hand, Gastrococos has
exclusively trichomosulcate pollen with reticulate
exine, but the aperture margin is not well differ-
entiated (M. Harley, pers. comm.). Elaeis pollen is
known from the Miocene (11-22.5 mya) from West
Africa (Muller, 198

A fossil of middle Eocene age, Astrocaryum ols-
soni, was discovered by A. Olsson in Negritos in
northwestern Peru. These calcified asymmetrical
nuts range from 3.75 to 5.25 ст in length and 2.5
to 3.75 cm in diameter and have a fibrous outer
layer, an inner layer 2-3 mm thick, and an interior
filled with structureless calcified material (Berry,
1926a). Other fossil endocarps aged between 12
and 45 Ma have been found in Boulder Hill, Otago,
and Wharekuri, Canterbury, New Zealand; they are
3.5-12 cm long and have distinctive Cocoeae pores
(Campbell et al., 2000). Berry (1926b) and Couper
(1952) reported Cocos-like fossils from Cooper's
Beach, Mangonui, Auckland, New Zealand, that are
from the Miocene period. The endocarps of the fos-
sil Cocos zeylandica (15-12 mya) resemble closely
those of the extant Parajubaea torallyi (Campbell
et al., 2000). Fliché (1896) described a fossil fruit
named Cocopsis from the Argonne of France of Mio-
cene age.

Fossil Cocos fruit from Chinchilla Sand, Queens-
land (Australia), of the latest Pliocene (2 mya), most
resembles the extant Cocos nucifera (Rigby, 1995).
The silicified fruit (10 cm long X 9.5 em max.
diam.) with three pores was also associated with
other silicified palmwood and megafauna bones.
Kaul (1951) recorded Cocos sahni embedded i
diatomous deposits from the early Tertiary (Eoce 5
in the mines at Kapurdi, Western Rajasthan, India.
Patil and Upadhye (1984) described a petrified fruit
of Cocos intertrappeansis from the Tertiary of Moh-
gaonkalan, Madhya Pradesh. Tripathi et al. (1999)
illustrated a fossil fruit very similar to Cocos nuci-

Jera from the Tertiary of Amarkantak, Madhya Pra-

desh. It is much larger than the others from India,
measuring 13 X 10 X б cm with a thin epicarp,
wide and fibrous mesocarp, and well-developed
hardened endocarp.

The now extinct Paschalococos disperta from
Easter Island was described by Dransfield et al.
(1984). Its fruits are very similar to those of the
extant Jubaea chilensis from Chile. About 30 par-
tially gnawed endocarps were discovered in the
cave floor near Ana Okeke, Easter Island. Four of
the best preserved fruits are about 2.5 X 3 em, with
smooth endocarps and three equatorially placed
pores. Radiocarbon dating aged them at about 820
+ 40 years В.Р,

BIOGEOGRAPHY

This well-documented Cocoeae fossil assemblage
suggests that Cocos nucifera is part of a lineage of
palms with former worldwide distribution. At pres-
ent most Cocoeae (201 species) are centered in the
Neotropics, with four species in the Old World (Af-
rica and Madagascar), while Cocos nucifera is pan-
tropical. The origin of the coconut has been a con-
troversial issue for more than a century because of
this biogeographical distribution. Alphonse de Can-
dolle (1886) and Cook (1910) proposed a New
World origin, Beccari (1963) claimed an Asiatic or

—

Polynesian origin, Moore (19730) presented evi-
dence for a Melanesian origin, Harries (1978) pos-
tulated that the coconut originated in the Western
Pacific. The question of dispersal by water and hu-
mans further complicates matters. Here, I attempt
to reconstruct the evolutionary history of Cocoeae
and in particular of the coconut. Estimated times
of divergence of the Cocoeae clades in the ML tree
using the Non Parametric Rate Smoothing (NPRS)
analysis (Sanderson, 2002) are calibrated with fos-
sil fruits, and the geographical distribution of Co-
coeae is mapped on the maximum likelihood tree
to suggest a possible model for the origin of Cocos
nucifera.

The Malagasy clade (Beccariophoenix and Voan-
toala) and the African Elaeis guineensis are both
basal in all analyses herein (Figs. 1—3) in the non-
spiny and spiny clades, respectively. Beyond this
clade, the majority of the non-spiny and spiny
clades are Neotropical. Basal to these two groups
is Barcella, a South American endemic Cocoeae.
Both outgroups, Reinhardtia (subtribe: Malortiei-
nae) and Roystonea (subtribe: Roystoneinae), are
Neotropical and belong to the palm tribe Areceae.
The topology therefore suggests a Neotropical origin
for the Cocoeae and for the wild progenitors of Co-

Volume 91, Number 3
2004

Gunn
Phylogeny of Cocoeae

cos nucifera. This hypothesis may be tested with
the times of divergence of the clades and tectonic
events.

At circa Eocene (55-37 mya) fossil Cocoeae
fruits were present in South America, New Zealand,
and India; Miocene (22—5 mya) endocarps have
been found New Zealand and Africa, Pliocene
(5-2 mya) fruits in Australia and India, and recent
partial endocarps (800 years old) on Easter Island.
By the Eocene Cococeae were already in existence,
and therefore probably arose as a lineage sometime
earlier, quite possibily the late Paleogene (65—60
mya) since palms were already well diversified as
evidenced by the fossil records (Raven & Axelrod,
1974; Muller, 1979: McLoughlin, 2001).

The chronogram (not shown) from the NPRS
analysis suggests that the spiny and non-spiny co-
cosoids diverged between 50 and 60 mya. Inde-
pendent estimates herein of the ages of these sister
clades are approximately the same, that of the for-
mer ranging from 42 to 46 mya and of the latter.
42 to 43 mva.

phoenix and Voanioala diverged from the rest of the

The two Malagasy genera Beccario-

non-spiny group ca. 40—51 mya (see herein, Table
2). The

Africa at about 90 mya, but there was possibly a

Madagascar block began separating from

connection between Madagascar and Africa until
2001). The
next cladogenesis was approximately 42 mya (see
herein, Л

the middle Oligocene (McLoughlin,

able 2), when the Cocos alliance became
differentiated from the Attalea alliance clade. Ju-
baeopsis caffra, the South African endemic, is with-
in this large non-spiny clade and estimated to have
diverged from the rest of the group about 36-38
mya. As South America and Africa had been sep-
arated by then, ca. 95-100 mya (Goldblatt, 1993:
23). it is quite possible that Jubaeopsis arrived in
Africa by long-distance dispersal. The fruit (2—4 cm
long) looks like a miniature coconut and possesses
a thin fibrous mesocarp covering a hard inner en-
docarp. It is restricted near the estuarine banks of
the Metentu, Msikaba, and Mzinlaua Rivers of the
eastern coast of South Africa (Tuley, 1995). The
distance between the southern tip of South America
and that of South Africa was not great during the
Eocene (Goldblatt, 1993), and the ocean currents
were moving westward (Axelrod & Raven, 1978).
Within the Cocos alliance, the age of the node
(chronogram, not shown) subtending Parajubaea is
at least 29.87-29.44 million years, and the node
closest to it subtending the crown group of Cocos
nucifera is aged at 22.20-26.84 million years (see
Table 2). Thus the minimum age of divergence of
Parajubaea and Cocos nucifera is approximately 23
million years. This finding suggests that the coconut

belongs to an ancient lineage with its wild progen-
itors occurring in the Neotropics, and it may be
possible that Cocos nucifera is the only extant spe-
cies of this lineage. Rigby (1995) reported a Cocos
nucifera fossil in Chincilla Sand, Queensland (Aus-
tralia), of Pliocene age (2 mya). This large fossil
Cocos has the three pores at one end distinctive of
the cocosoid palms. This also eliminates any action
of humans in the original distribution of Cocos nu-
cifera, although the dispersal of it in the Pacific in
recent times was partly the responsibility of hu-
mans. At the time of divergence of the putative pro-
genitors of the Cocos nucifera, separation of South
America from West Antarctica had already taken
place (30 mya) as the Powell Basin opened up the
Scotia Sea to create the Drake Passage (Hallam,
1981). The geological ages of the Cocoeae endocarp
fossils found in New Zealand fall into two groups—
Eocene and Miocene. The Eocene group found on
the eastern side of the South Island is postulated
here to have arrived from South America via the
Antarctic land bridge, but the Miocene group found
on the northern shores of the North Island persisted
till much later when New Zealand moved northward
resulting in subtropical climes in the North Island
during the Miocene. The emergence of volcanic ar-
chipelagoes to the north enabled the exchange of
subtropical taxa to and from New Zealand (Raven
& Axelrod, 1972).

The early lineage of Cocos nucifera most likely
possessed some means of water dispersal. The fruit
of Cocos nucifera differs most prominently from
those of other Cocoeae in its large size, thick layer
of fibrous mesocarp, and its large endocarp with a
huge cavity lined with a layer of hard endosperm
and filled with liquid endosperm. This adaptation
for floating and the enclosed vessel protecting the
developing embryo would probably enable it to
cross ocean barriers and establish successfully. Ed-
monson (1941) suggested that the coconut can float
in the ocean for up to three months and still be
viable.

It may be hypothesized that Cocoeae may have
originated in South America during the Paleogene,
Africa,

gascar, and India and southward to Australasia and

diversified and spread eastward Mada-
New Zealand through the western Antarctic corri-
dor (till the Oligocene). The putative progenitors of
the coconut were from South America and became
widely distributed in the Old World by long-dis-
ance water dispersal.

~

The Deccan Traps of India
have a well-studied paleobotanical flora (Prakash,
1958) and show affinities to those of the Gondwan-
an continents. It is postulated that Cocoeae mi-

grated India from Madagascar after the diver-

Annals of the
Missouri Botanical Garden

gence of the basal clade via long-distance dispersal

as the fossil endocarps found in India were of lower

Eocene age, when India had already separated from
Madagascar. These fossils were described as having
fibrous mesocarps (see Patil & Upadhye, 1984, and
Tripathi et al., 1999)

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Volume 91, Number 3 Gunn 521
2004 Phylogeny of Cocoeae

Appendix l. Species sequenced and collection data. Sampling method: Every extant known palm genus (20) in the

Cocoeae was sampled. In several genera two or more taxa were listed. One dwarf and two tall forms of Cocos nucifera

were sequenced.

Taxon

Herl vari um voucher

GenBank access. no. prk

Extant:
Acrocomia aculeata (Jacq.) Lodd.
Acrocomia media O. F. Cook

Aiphanes aculeata Willd.

Aiphanes caryotifolia (Kunth) H. Wendl. syn.

Aiphanes ac uleata ta

Aiphanes minima (Gaertn.) Burret
Allagoptera arenaria (Gomes) Kuntze
Allagoptera leucocalyx (Mart.) Kuntze
Astrocaryum gynacanthum Mart.

Astrocaryum paramaca Mart.

Attalea cohune Mart.

Attalea cuatrecasana (Dugand) Henderson,
;aleano & Bernal

Attalea А Вањ. Rodr.

Attalea speciosa Spreng.

Attalea phalerata Spreng.
Bactris maraja Mart

Barcella odora (Trail) Drude
Beccariophoenix madagascariensis Jum. &

Perrier

Весе.

ка,

Butia capitata (Mart.
Butia ertospatha (mart.) Весс.
Cocos nucifera L. (dwarf)

Cocos nucifera L. (tall)

Cocos nucifera L. (tall)

Desmoncus chinantlensis Liebm. ex Mart.
Elaeis guineensis Jacq.

Elaeis oleifera (Kunth) Cortés
Gastrococus crispa (Kunth) Н. К. Moore

Jubaea chilensis (Molina) Baillon

Jubaeopsis caffra Beccari

Brazil, Henderson AH 3057 (NY)
Puerto Rico, Gunn 2 (MO)

Brazil, Henderson AH 3072 (NY)
Brazil, Gunn 90 (MO)

Cuba, Gunn 95 (MO)

(Lewis & Doyle, 2002)

Brazil, Gunn 93 (MO)

French Guiana, Torke 239 (MO)
French Guiana, Torke 238 (MO)

Belize. Gunn 69 (MO)
Colombia, Henderson AH 3069 (NY)

Brazil, Noblick 5133 (MBC)
Brazil, Henderson AH 3067 (NY)

razil, Noblick 5018 (MBC)
Colombia, Bernal, Galeano, Sanders
1096 (FTG)
Brazil, Kahn 3608 (CEN)
Madagascar, Noblick 5065 (MBC)
Brazil, Henderson AH 3064 (NY)
Brazil, Gunn 87 (MO)
Cult. (tropical Melanesia), Gunn 85
(MO)
Cult. (Pacific), Gunn 86 (MO)
Pacific, Henderson AH 3063 (NY)
Guatemala, Hubbuch & Aronson 120
FTG
Cult. (MBC), Gunn 88 (MO)
South America, Gunn 94 (MO)
Cuba, Zona 614 (FTG)

Chile. Henderson 3073 (NY)

South Africa, Brand 452 (NY)

AY601224

AY601222 (Clone Al)
AY601223 (Clone A2)
AY601210

AY601211 (Clone B)
AY601207 (Clone Al)
AY601208 (Clone A2)
AY601209 (Clone A3)
AY601206 (Clone Al)
AF453331

AY601242 (Clone Al)
AY601227 (Clone Al)
AY601228 (Clone A2)
AY601213 (Clone Al)
AY601229 (Clone A2)
AY601239 (Clone A)
AY601241 (Clone A)

AY601238

AY601245 (Clone AI)
AY601246 (Clone A2)
AY601240 (Clone A)
AY601214 (Clone A)

AY601215 (Clone AI)
AY601216 (Clone A2)
AY601217

AY601236 (Clone Al)
AY601237 (Clone A2)
AY601251 (Clone Al

AY601253 (Clone Al
AY601254 (Clone A2)
AY601230 (Clone Al)
AY601231 (Clone A2)
AY601232 (Clone B1)
AY601233 (Clone B2)
AY601234 (Clone C)

—

AY601235
AY601212 (Clone A)

AY601219 (Clone Al)
AY601220 (Clone A2)
AY601221 (Clone A3)
AY601218

AY601225 (Clone A)
AY601226

—

AY601255 (Clone A1)
AY601256 (Clone A2)
AY601257 (Clone АЗ
AY601258 (Clone A4
AY601272 (Clone A)
AY601273

= МУ

522

Annals of the
Missouri Botanical Garden

Appendix l. Continued.

Taxon

Herbarium voucher

GenBank access. no. prk

Lytocaryum weddellianum (H. Wendl.) Tol.

Parajubaea torallyi (Mart.) Burret

Polyandrococcos caudescens (Mart.) Barb.
Rodr.

Syagrus amara (Jacq.) Mar

Syagrus romanzoffiana (Cham.) Glassman

Syagrus smithii H. E. Moore

Voanioala gerardii J. Dransf.

Outgroups:
Reinhardtia gracilis
Roystonea regia

Fossil Fruits:

FI Wharekuri
F2 Boulder Hill
F3 Waihao husk

F4 Cocos intertrappeansis

Brazil, Henderson AH 3059 (NY)
Bolivia, Vargas 3183 (NY)
Brazil, Noblick 5003 (MBC)

Dominica, Noblick 4809 (MBC)
Brazil, Henderson AH 4210 (NY)

Peru, Noblick 96260 (MBC)

Madagascar, Dransfield J. D. 6389 (К)

(Lewis & Doyle, 2002)
(Lewis & Doyle, 2002)

New Zealand, Fordyce OU 30758 (Otago
Univ., Dunedin)

New Zealand, Millan, Stillwell & Linqu-
ist OU 31113 (Otago Univ., Dunedin)
New Zealand, Gebneff, OU 39784 (Otago

Univ., Dunedin
India, Pati! MOH/EVU/16 (Inst. Sci.,
Nagpur)

AY601249 (Clone A)
AY601250

AY601264 (Clone Al)
AY601265 (Clone A2)
AY601243 (Clone Al)
AY601244 (Clone A2)
AY601259 (Clone A)
AY601247 (Clone Al)
AY601248 (Clone A2)
AY 601260 (Clone н
AY601261 (C
AY601262 (Clone АЗ)
AY601263 (Clone А4)
AY601266

AY601267 (Clone Al)
AY601268 (Clone A2)
AY601269 (Clone A3)
AY601270 (Clone A4)
AY601271 (Clone A5)

АК453372
AF453375

Volume 91, Number 3, pp. 369-522 of the ANNALS OF THE MISSOURI BOTANICAL GARDEN
was published on October 20, 2004.

ШО

www.mbgpress.org

CONTENTS

Pollination Ecology of Gaura and Calylophus (Onagraceae, Tribe Onagreae) in Western
exas; U.S.A

PAPE ME -Richard R. Clinebell II, Angela Crowe, David P. Gregory & Peter C. Hoch

A иншә Overview of Frankeniaceae and Tamaricaceae from Nuclear rDNA and Plastid

Sequence Data John F. Gaskin, Farrokh Ghahremani-nejad,
Dao-yuan Zhang & Jason P. Londo

Revision of the Madagascan Endemic Stapelianthus (Apocynaceae) Based on Molecular
and Morphological Characters P. V. Bruyns & C. Klak

Phylogeny and Evolution of Symbolanthus and Wurdackanthus (Gentianaceae—Helieae) in
the Guayana Highlands and Andes, Based on Ribosomal 5S-NTS sequences

Katherine R. Gould & Lena Struwe

ҮШ International Aroid Conference, Missouri Botanical Garden, St. Louis, 9-11 August
999 Introduction Thomas B. Croat
Synopsis of the Genus Spathiphyllum (Araceae) in Colombia Felipe Cardona
Araceae from Central Brazil: Comments on Their Diversity and Biogeography =

: Eduardo G. Goncalves

Progress in Ornamental Aroid Breeding Research

R. J. Henny, D. J. Norman & J. Chen

A Preliminary Survey of Petiolar Collenchyma in the Araceae

Eduardo G. Gonçalves, Elder А. S. Paiva & Marcus A. Nadruz Coelho

Vegetative Anatomical Data and Its Relationship to a Revised Classification of the
Genera of Araceae | Richard C. Keating

Systematic Occurrence of Raphide Crystals in Araceae _......... -Richard C. Keating

The Phylogeny of the Cocoeae (Arecaceae) with Emphasis on Cocos nucifera Bee Е Gunn

Cover illustration. Trisetum ligulatum Finot & Zuloaga, drawn by Vladimiro Dudás.

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Volume 9] Annals
Number 4 of the
2004 Missouri

Botanical

Garden

AFRICA'S HOTSPOTS OF Wolfgang Kiiper,?” Jan Henning Sommer,”

BIODIVERSITY REDEFINED! Jon C. Lovett, Jens Mutke,? Hans Peter
Linder," Henk Jaap Beentje,’ Renaat
Sylva Angèle Rosine Van Rompaey,”
Cyrille Chatelain,’ Marc Sosef,* and
Wilhelm Barthlott?

ABSTRACT

key problem for conservation is the coincidence of regions of high biodiversity with regions y ae human impact.

Twenty- five of the most threatened centers of plant diversity were identified by Myers et al., anc “hotspots” play
a crucial role in 5 conservation strategies. The primary goal of the hotspots is to cover rhe most dead ned
centers of plant diversity, but their efficacy has not yet been tested empirically. For sub-Saharan Africa, our study

evaluates the йер. 1 by Myers and compares them to a set of rede fined MES ы on the basis of
mappe ed distribution data for 5985 plant species. The two sets of hotspots overlap by 48%. Our redefined hotspots
include 80% of the species and 66% of the range-restricted species of the sub-Saharan ii in areas under high human

! Data compilation, as well as the coordination of the merged databases at the Nees Institute for Biodiversity of
Plants in Bonn, are funded by the German Federal Ministry of Education and Research (BIOLOG BIOTA Programme,
ainz, and supporte d by the University

—

WWW. Mp afric a.org). and the Akademie der Wissenschaften und der Literatur.
of Bonn. CABS—Conservation International and the Danish Centre for Tropical Biodiversity (University of Copenhagen,
Eo funded the plant compilation work in York. in particular for James ‘Taplin. The Danish Centre for Tropical
Biodiversity and various other funds supported data compilation in Denmark, in particular for Anne-Marie Biirger and
Christian Frimodt-Moller. We thank the numerous experts who contributed to the plant data used in this paper, in
particular Patricia Craven (Windhoek), Laurent Gautier (Geneva), Tony Rebelo (Kirstenbosch), Jeróme Degreef (Meise),
Peter Frankenberg (Stuttgart), Don Kirkup (Kew), Norbert Jiirgens (Hambur rg), Sigrid Liede (Bayreut th), Hager Вар
(Кем), Adjima Таана (Ouagadougou), Mauricio Ve n and Fernando Casas (Madrid), Jan W ninge
and Georg Zizka (Frankfurt). Paul Williams of The Natural History Museum, London, provided the WORL DM. Ар
software. Jan Schnitzler (Bonn) assisted with the manusc нен We thank > rold Kier jrn Tony Rebelo (Kirstenbosch),
Paul Williams, и two anonymous reviewers for valuable comments on the manusc
Nees Institute for Biodiversity of Plants, University of Bonn, Mec ie nheimer Allee 170. D-53115 Bonn, Germany.
ыл m de
e for Ecology, Law and Policy, Environment Department, University of York, Heslington, York, YOIO 5 DD,
йык! Кыш Я
Institute of Systematic Ea Zollikerstrasse 107, CH-8008, Zurich, Switzerland.
^ Royal Botanic Gardens . Richmond, Surrey TW9 3AE, United Kingdom.
^ Université libre de i 5 1 LB, Laboratoire de Botanique systématique et Phytosoc iologie, 50 Av. F. D. Roosevelt
1050 Bruxelles, Belgium.
Conservatoire et Jardin botaniques de la Ville de Geneve, case postale 60, CH-1292 Chambesy, Switzerland.
* National ais a x the Netherlands- Wageningen branch. Biosystematics Group. Wageningen University, Ge-
neraal Foulkesweg 37. 3 BL Wageningen, The Nethe rlands.
" Corresponding ша

ANN. MISSOURI Вот. GARD. 91: 525-535. 2004.

526

Annals of the
Missouri Botanical Garden

impact, whereas ei values are 15% and 11% lower for Myers’s hotspots. Despite having equal size and a considerable

spatial overlap with V
in i Мариш d е
and the Albertine Rift. Мапу о

1 Katanga, the

Their еа is essential S a comprehensive coverage
Iss /

ey wore
important plant areas

yers's hotspots, our ir fine á hotspots include further highly threate ned centers of plant diversity
East A
these re le fined. 1 are [з protec led centers of E and animal diversity.

frican Afromontane region, the Lower Guinea Region,

—

Africa’s centers of biodivers

‚ biodiversity, conservation, endemism, G lobul Strategy for Plant Conse rvation (GSPC), hotspots,

There are growing concerns about the coinciding
spatial patterns of human population density and
biodiversity (Cincotta et al., 2000; Myers et al.,
2000; Balmford et al., 2001; Luck et al., 2004). In
a pioneering study in 1988, Myers identified a glob-
al set of hotspots where exceptional concentrations
of species with high levels of endemism face ex-
ceptional threats of destruction (Myers, 1988). Lat-
er updates (Myers, 1990; Myers et al., 2000) played
a crucial role in the public perception of the threat
to biodiversity and the development of large-scale
concepts for setting spattal priorities for in situ con-
servation, as required by Article 8 of the Conven-
tion on Biological Diversity (UNCED, 1992).

Whereas centers of diversity are identified on the
basis of biological richness and endemism, the hot-
spots concept of Myers et al. (2000) combined two
criteria: plant diversity and the threats to that di-
versity. In practice, hotspots were defined as areas
with less than 30% intact primary vegetation and
with at least 0.5% of the global plant species being
endemic to the area

yers et al. based their study on two types of
information. In addition to expert advice, they used
summary information on the number of endemic
species occurring in the hotspots. This “inventory-
based type" of information (Barthlott et al., 1999;
Mutke et al., 2002) was the only available infor-
mation on the biodiversity for many areas (Myers
et al., 2000; Krupnik & Kress, 2003), though the
application and the analysis of this data type is
limited (Mutke & Barthlott, in press). Indeed, My-
ers et al. (2000; see also Brooks et al., 2001) men-
Africa for

which the available data are insufficient to decide

tioned several areas in sub-Saharan
whether or not they represent a hotspot. They also
stated that due to the heterogeneous data situation,
they had to use the endemism criterion even though
it was felt to be (Myers et al., 2000).
In addition, information on biodiversity was, and

“minimalist

often still is, only available for comparatively large
areas delineated by political boundaries. This low
spatial resolution limits the accuracy to which cen-
ters of diversity can be identified (Krupnik &
Kress, 2003).

More than a decade after the first global set of

hotspots was published, it has become possible to
define hotspots more rigorously and accountably.
"laxon-
1999;
Mutke & Barthlott, in press), consisting of reliable

Diversity can now be calculated from a

based type” of information (Barthlott et al.,
data on the individual distribution areas of a large
number of taxa (Williams, 1996; Burgess et al.,
1998). New high-resolution socioeconomic data
(CIESIN, 2000; Sanderson et al., 2002) have be-
come available. Complex algorithms (Margules &
Pressey, 2000) allow a more precise identification
of centers of richness and endemism (Lovett et al.,

2000;
of the degree of potential conflict between conser-

Linder et al., in press) and permit analyses

vation and land-use interests (Balmford et al.,
2001; Williams et al., 2003; Luck et al., 2004).

Consequently, taxon-based biodiversity informa-
tion has been used to criticize the global hotspot
areas as defined by Myers et al. (2000) for their
conceptual background (Jepson & Canney, 2001),
for their performance in comparison to other area
networks selected on more complex parameters
(Williams et al., 1996; Balmford et al., 2001), for
their size (Brummit & Lughadha, 2003), and oc-
casionally for their location (Burgess et al., 2002;
Krupnik & Kress, 2003). However, to our knowl-
edge, there is no study that assesses whether the
hotspots do indeed cover the most threatened cen-
ters of plant diversity, even though this was the
original intention of this prioritization scheme.

In this paper we evaluate the extent to which
Myers’s hotspots include a maximum number of
rare plant species in those areas most threatened

by human impact in Africa. This is important for

—
—

four reasons: (i) as the foundation of food webs,
plants are of essential importance for terrestrial
biodiversity; (ii) plants might be the best available
surrogate to represent invertebrate diversity (Myers,
1988); (111) plant diversity is insufficiently covered
by current networks of protected areas (Burgess et
al. in press); and (iv) plants are the group from
which hotspots were identified by Myers et al.
Which criteria should be used to evaluate and
enhance the performance of the hotspots? A mod-
ification of the current hotspots would be desirable
if they exclude areas in which more rare plant spe-

Volume 91, Number 4
2004

Kuper et al.
Africa’s Biodiversity Hotspots

cies are more threatened by human impact than in
included areas. Here we test the efficacy of the
hotspots using the most comprehensive available
database of plant species distributions for sub-Sa-
haran Africa.

METHODS
SPECIES DATABASE

Since 2003, an international group of research
institutions has contributed data on Africa-wide
plant distributions to the Biogeographic Informa-
tion System on African Plant Diversity (BISAP),
which 15 hosted and curated by the BIOMAPS Proj-
ect within the BIOLOG BIOTA framework (www.

biota- africa.org).

—

‘he database includes Africa-wide distribution
records for 6269 species (status March 2004). all
of which had been taxonomically revised. The da-
tabase comprises about 330,000 distribution rec-
ords from confirmed collection localities. The spa-
lial precision of the data varies from exact localities
(mainly from herbarium collections with geo-refer-
enced localities) to one-degree resolution data from
digitized maps. Data are organized in MS Access
databases and have been plotted and analyzed us-
ing WORLDMAP software (Williams, 2002) and
Arc View 3.2a GIS software (ESRI, 2000). In order
to achieve maximum comparability with previous
analyses on sub-Saharan zoodiversity (Balmford et
al., 2001; Brooks et al., 2001; Burgess et al., 2002;
Burgess et al.. 2004: De
Klerk et al., 2004), all plant distribution data were
rescaled to a one-degree grid resolution within a

in press: Fjeldsà et al..

base map of 1713 one-degree latitude-longitude
Africa

south of 17 degrees latitude. By restricting the geo-

grid cells covering mainland sub-Saharan

graphic coverage to Africa south of the Sahara and
excluding those species found only on offshore is-
lands, a database with 5985 plant species remains
This is between 10% and 15%
of the species in the African flora (Lebrun & Stork,
1991-1997; Beentje et al., 1994).
formation on the origin of this data set is docu-

for further analyses.
Additional in-
mented in Burgess et al. (in press, see also footnote

Our plant data are the most comprehensive ever
assembled for the study area, but inevitably have
limitations. There are certain areas in Ethiopia and
Somalia, Sudan, the Central African Republic, the

Republic of Congo. the Democratic Republic «

-

Congo, and Angola where analysis of sampling in-
tensity indicates that plant diversity is not ade-
quately documented in our databases (W. Küper.

unpublished. data). The scientific exploration «

f

~

these areas is an important challenge for the future.
Inadequate availability of distribution data could
have two effects on our analysis: First, in cases
where we have inadequate data for areas included
in the hotspots as delineated by Myers et al. (2000),
testing the hotspots on the basis of our data might
result in an underestimation of their performance
in covering sub-Saharan plant diversity. However.
in fact the most detailed, updated, and comprehen-
sive. distribution data in our database is for those
areas covered by the Myers’s hotspots (which may
partly be a consequence of highlighting these areas
since 1988): (1) Data for the upper Guinea (West
Africa) hotspot stem from the National Herbarium
of the Netherlands-Wageningen branch: (ii) data for
the Western Cape are from the National Botanic
Institute, Republic of South Africa, and contributed
by Л. Rebelo and N. Jürgens: and (iii) distribution
data for East Africa stem from a compilation of re-
stricted-range species for the area of the Flora of
Tropical East Africa (Н. Beentje, unpublished data,
together with other sources). Even though the data
for West Africa are comparatively comprehensive,
the eastern part of the upper Guinea hotspot is po-
tentially less well represented due to lower data
availability. Second, it is possible that the selection
of our alternative set of hotspots on the basis of our
data misses areas that are richer in species than
those included simply because the former ones are
not adequately collected. This is certainly a key
problem if areas are selected on the basis of species
richness alone. But this problem is not as promi-
nent when selecting hotspots, because their iden-
tification is also based on the intensity of human
impact. Hotspots tend to be particularly well col-
lected (i) due to their popularity with biologists
(Reddy & Davalos, 2003) and (ii) because their
high human impact is associated with a compara-
tively good wr providing access (Gibbs
Russell et al.,
DIGITIZING THE HOTSPOTS OF MYERS ET AL.

In order to compare the sub-Saharan hotspots of
Mvers et al. (2000) with our data arranged in one-
degree cells, we first digitized Myers’s hotspot poly-
gons (delineations taken from Mittermeier et al..
1999
then identified all cells that had a spatial overlap

—

and overlaid them on our grid of cells. We

of more than 25% of their area with the hotspots
|
2002). The

decision to accept or omit cells with less than 25%

polygons (see methods in Burgess et al..

overlap could affect the performance of the hotspots
Africa's

plant diversity compared to alternative hotspots de-

T most threatened. centers. of

i>)

covering

528

Annals of the
Missouri Botanical Garden

N с
о о
4 J

Range Size Rarity (%)
e

0 +

Human Footprint (96)

Figure l. Scatterplot illustrating the values of range-size rarity and mean ане ha Hk (rescaled from Sanderson
et al., 2002) for each of the 1713 + ub: Saharan one-degree cells (each re prese nte a black i pens concealed by
other symbols). Both paramet re rescaled to percentages. For better visualiz ition, th ' seven lis ith a range-size
rarity of more than 30% are not shown (X/Y-values for here ce "nm (63/100), (15/89), (99/68). опоо, (38/42), (53/36)
(42/35)—these are all in both Myers hotspots and redefined hotspots). Open 25 cells ed by the Myers
hotspots. Gray boxes: 125 cells with highest product of range-size rarity oa die uod. cited as "redefined

hotspots” in the text.

lineated on the basis of our data. We therefore test-
ed whether the inclusion of further cells (those with

ess than 25% overlap) would improve the perfor-
mance of the hotspots in comparison to our rede-
fined hotspots of equal area in each case. If this
was the case, we accepted the cell as part of the
hotspots. With this most conservative method in fa-
vor of the performance of the Myers et al. hotspots,
125 cells were identified as being part of these hot-
From here on,

spots. they will be referred to as

“Myers hotspots” (Fig. 2A).
CHOOSING DATA
AND ITS THREAT

TO REPRESENT PLANT ENDEMISM

The aim was to select data to best approximate
the two criteria used for the delineation of the My-
€

ers hotspots, which were plant endemism and

threat. Using our data we selected 125 cells

which plant diversity and threat are maximized
(Fig. 1) on the basis of the following two measures.
(i) We calculated range-size rarity for each cell (Fig.
2B). This combines the number and range sizes of
species in each cell (Williams, 1996; Kier & Barth-
lott, 2001; Wieringa & Poorter, 2003).
species that occur in a cell and the smaller their

The more

ranges are, the higher the value. We chose range-
size rarity since it best approximates the endemism
criterion applied by Myers et al. (2000). In contrast
to their criterion, range-size rarity includes not only
the species strictly endemic to the hotspots, but
also every species whose range overlaps with them.
Hence, two areas with the same number of strict
endemics can still be differentiated according to
their contribution in covering the ranges of other
species. (ii) As a surrogate for threat, we calculated
the mean human footprint for each cell, rescaling
the data from Sanderson et al. (2002) to one-degree
cells (following the methods used in Balmford et
2001; Luck et al., 2004). For coastal cells, the

mean footprint was calculated on the basis of main-

al..

land values only. The human footprint index shows
similar spatial patterns to parameters such as pop-
ulation density, which was used in previous studies
(Balmford et al., 2001: Lesslie, 2002: Luck et al.,
2004). n addition takes into consideration a
wider range of factors, such as infrastructure and

but i

land-cover. Thus, agricultural areas that do not nec-
essarily have a high human population density are
included as having a high human impact оп bio-
We

diversity. calculated mean values of human

Figure 2.
de line ated by Myers et al. (2000). Solid black line within co
grids cove red by the Myers hotspots (see methods). Red
A ie product of ra
Table 1) of a near-minimum-cost area set (Willia
—B. Range-size rarity per one-degree grid cell.

nge-size rarity and mean Seas 2.

the species occurring in each cell. It is calculated as the

squares:

This i measure combines the values for richness and the range sizes «

E

—A. Map of the set of redefined hotspots identified in the present study, contrasted with the hotspots as

ntinent: Myers hotspots. Gray open squares: 125 one-degree
‘ls covered by the re defined лш (cells with
int per ce In. Black dots represent 125 first cells (c ms
the entire near-minimum-cost set is illustrated in Fig. 2B).
Y

sum of the inverse range sizes per cell (Williams, 1996).

pr

Volume 91, Number 4 Kuper et al. 529
Africa’s Biodiversity Hotspots

20°
10° 10°
0° 0°
10° 10°
20° 20°
30° 30°
20°
20°
10° 10°
0° 0°
10° А Р 10°
range-size rarity
иш high
a
*
20·˙ [ 20°
medium
E
aum
mm
30° 30°
low
20° 10° 0° 10° 20° 30° 40° 50°
Figure : —B. (Continued) Note that many species of medium range size may result in a similar cell value as one
with fewer species of very small range size. Black dots mark 422 cells that form the near-minimum-cost area set for

sub-Saharan plant diversity in the data set (Williams, 2002). These cells represent all 5985 plant species in a set with
near-minimum total. human footprint. The figure shows Africa south of 17?N latitude with grey background. lines

indic 'aling national boundaries.

530

Annals of the
Missouri Botanical Garden

footprint per cell so that roads or populated places
close to relatively intact areas do not dominate the

values for these cells. From here on, mean footprint
per cell is referred to as “human footprint.”

IDENTIFYING HOTSPOTS ON THE
DATA

BASIS OF OUR

(i) Range-size rarity and human footprint were
normalized to a percentage of their maximum value,
so that they are both equally scaled.

(11) To represent a measure that best approxi-
mates the “heat” of the Myers hotspots, we then
calculated the product of the value of footprint and
range-size rarity. This index, which combines bio-
diversity and human impact, does not fully repro-
duce the methods of Myers et al. and is too sim-
plistic to derive any detailed conclusions on
conservation priorities. However, it is suitable for
representing the degree of potential conflict be-
tween the conservation of diversity and pressure on
land use resulting from existing human activities
(Fig. 1, compare methods used by Balmford et al..
2001: Luck et al.,

that both range-size rarity and human footprint

2004). Using the product ensures
must have comparatively high values to obtain a
high combined index value.

(111) The 1713

ranked on the basis of the square-root values of the

sub-Saharan cells were then
combined index for each cell.

(iv)

were selected. We chose only 125 cells so that their

The top 125 cells with the highest values

total area approximates to the total area of the My-
ers hotspots. From here on, the 125 cells selected
on the basis of our data will be referred to as “re-

defined hotspots? (Fig. 2А).

COMPARING THE
ALTERNATIVE

PERFORMANCE OF THE
SETS OF

TWO
HOTSPOTS

Although the redefined hotspots cover the 125
cells with the highest product of range-size rarity
and human footprint, this does not necessarily
mean that they must include more rare species in
total,

ranges than do the Myers hotspots. To compare both

or indeed a larger proportion of the species?

sels of hotspots, we applied three tests: (i) How
many species are included? (ii) How many species
belonging to the quartile of species with most-re-
1994) are included?

(iii) Which proportion of the ranges of the sub-Sa-

stricted ranges (see Gaston,

haran plant species is covered? The latter measure
is calculated by summarizing the values of range-
size rarity for all cells included in each set (anal-
C-value of Kier & Barthlott, 2001).

From here on this measure is referred to as

ogous to the

eu-

mulative range-size rarity.” The parameters tested
were considered to be the best measure of any set
of areas to fulfill the original aims of the Myers

hotspots.

HOTSPOTS AS CONSERVATION PRIORITIES?

The Myers hotspots are promoted as a network
of areas suitable to “protect the most species per

(Myers et al., 2000).
bles the goal of recently applied heuristic selection

dollar invested” This resem-
algorithms for seeking near-minimum-cost area sets
(Gaston, 1994). The latter type of area sets repre-
sents each species at least once, but tends to min-
imize the hypothetical "costs" of potential conser-
vation actions by choosing cells with, for example.
2001: Wil-

or at least cost (Moore et al.,

least human impact (Balmford et al.,
2003),

2004). The approach aims to alleviate conservation

liams et al.,

conflicts where there is scope for this (Luck et al.,
2004).

mum-cost area set counts the number of rare spe-

Technically, the algorithm for. near-mini-
cies in each cell (after taking floristic complemen-
tarity with previously chosen cells into account)
and then divides the diversity score for each cell
by the human footprint value of the respective cell.
Such a near-minimum-cost area set was calculated
on the basis of the same parameters used for the
hotspots analyses. We then selected the 125 cells
ıaving the highest benefit-to-cost ratio and con-
trasted them with the Myers hotspots and the re-
l, Fig. 2A,

defined hotspots (Table

RESULTS

There is a substantial spatial overlap (Figs. 1, 2)
between the Myers hotspots and the redefined hot-
spots identified on the basis of our data. The top
17 redefined hotspot cells are included in the My-
A total of 60 out of the 125
cells covered by the Myers hotspots are also iden-

ers hotspots as well.

tified as redefined hotspots.

The 125 cells in the Myers hotspots include
3841 of the 5985 sub-Saharan plant species rep-
resented in our database (Table 1). Fifty-two per-
cent of the species belonging to the quartile of spe-
cies with most restricted. ranges are included.
Cumulative range-size rarity for all cells is very
high, with 39% of the maximum cumulative value
for all 1713 sub- ‘he average human
footprint among the 125 cells is 24.32; similar val-
ues are measured in cells covering cities such as
Kigali, Kisangani, or

Saharan cells. '

Bloemfontein. Values higher
than 30 are characteristic of metropolitan areas
such as Durban, Cape Town, Dar es Salaam, Abi-

djan, and Douala.

Volume 91, Number 4 Kuper et al. 531
2004 Africa’s Biodiversity Hotspots
Table Comparative performances of three area sets of equal size to cover the sub-Saharan centers of plant

je
diversity. The following sets are compared: the hotspots as defined by Myers et al. (2000). a redefined set of hotspots
identified on the basis of distribution data for 5985 plant species, and a near-minimum-cost area set on the basis of
the same data. In order to рр the sets, all have been rescaled to а one-degree based grid of 1713 cells covering
Africa south of 17° latit i)
number of restricted range 1 covered: (iii) cumulative range-size rarity for the included cells: and (iv) human
Percentages indicate the proportion of the respective total values for

The comparison is based on four criteria: (i) overall number of species covered: (i

footprint (sum and average for the included cells).
sub-Saharan Africa, The plant data stem from the Biogeographic Information System on African Plant Diversity (BISAP)
representing 10%—15% of the species of the sub-Saharan African flora. Note that the aim of hotspot sets is to cover
the most threatened centers of plant diversity (represented by high values for both plant diversity and human footprint).

whereas the near-minimum-cost area set seeks to cover all species in cells with a human footprint as low as possible.

Sub-Saharan

Africa Mvers Hotspots Redefined Hotspots Near-minimum-cost set
Total Total % Total % Total %
One-degree cells 1.713 125 7.3 125 7.3 2 Ta
MI species 5.085 3.841 61.2 1.759 79.5 5.196 80.8
Restricted-range species 1.540 802 52.1 1,011 05.6 1.155 15
Range-size rarity (sum) 2.985 2.354 39.3 2,955 9.4 2,003 13.5
Human footprint (sum) 33,905 3.040 — 3,420 — 2,215 —
Human footprint (average) 19.8 24.: 27.4 — 17.7 -—
However, the Myers hotspots exclude some of the Mts. and the coast in Gabon, the Mavombe center

cells with very high range-size rarity and human
footprint, and conversely include other cells with
comparatively low values for range-size rarity and
human footprint (Figs. 1, 2). In total, 65 cells of
the redefined hotspots do not coincide with the My-
ers hotspots (see below).

In an area of approximately the same size as the
Myers hotspots, the redefined hotspots include 15%
more of all species and 11% more of the rare spe-
cles occurring in our databases for sub-Saharan Af-
rica (Table 1): in total. that is about 80% of the
species included in our databases. Moreover, they
cover a 25.5% higher cumulative range-size rarity
than the Myers hotspots—and they do so in areas
that are characterized by a 12.5% higher total hu-
man footprint.

The redefined hotspots overlap with regional
centers of plant diversity not covered by the Myers
hotspots (Fig. 2A, В). In southern Africa these are
mainly cells in Maputaland, Pondoland, Barberton,
Sekhukhuneland, and Soutpansberg. In Katanga.
the Zambezi Source Area, Kundelungu and Upem-
ba National Park are important. In eastern Africa,
the Chimanimani Centre, Mt. Mulanje. a large
block of cells in the Albertine Rift including the
Kivu area, the Ruwenzori and Virunga Volcanoes.
Bwindi forest, Mt. Elgon, Mt. Kenya, as well
other areas with Afromontane or Afroalpine vege-
tation mainly in Kenya are among the redefined
hotspots (Fig. 2). The same is true for cells in the
lower Guinea forest block, including parts of south-
eastern Cameroon and the area between Crystal

of plant diversity. These areas have been identified
as centers of plant diversity before (for example.
1978: Beentje et al., 1994; Olson & Di-
nerstein, 1998; van Wyk & Smith, 2001)

The 125 cells selected for the near-minimum-

Brenan,

cost area set for sub-Saharan plant diversity have
an overlap of 58 cells with the redefined hotspots
(Fig. 2).

clusters of redefined hotspots contain cells with

The overlap is high because all regional

one-cell endemics. Although the algorithm seeks to
avoid hotspots and instead chose alternative cells
with a low human impact, this is not possible for
many cells because they are irreplaceable for rep-
resentation of their endemic species. Even though
the redefined hotspots have been delineated on the
basis of simplistic criteria and methods. the irre-
placeability of a considerable part of their area im-
plies that they will play an important role in more
complex and more adequate prioritizing schemes—
there are simply no alternatives in many cases.
However, the top 125 cells of the near-minimum-
cost area set include more species and more re-
stricted-range species than the Myers hotspots and
the redefined hotspots, even though they include a
set of cells with a much smaller total and average
human footprint. Bearing in mind the limited com-
parability and simplified assumptions of the algo-
rithm, this result indicates that, instead of priori-
tizing all hotspots as “conservation areas.” there is
potential to alleviate conservation conflicts in sub-

Saharan Africa by prioritizing areas with less hu-

532

Annals of the
Missouri Botanical Garden

man impact for conservation, such as, for example.

7

а rainforest block in central Gabon (see Fig.

DISCUSSION
A REDEFINED SET OF SUB-SAHARAN HOTSPOTS

The Myers hotspots cover 64% of all plant spe-
cies and more than half of the restricted-range plant
species included in our database for sub-Saharan

Africa.

Although this is an impressive performance for

only 125 cells (7

fined hotspots have an even higher representation

3% of the total area), the rede-
of the threatened sub-Saharan flora (Table 1). This
is mainly due to the fact that some important cen-
ters of plant diversity under high human impact are
not included in the Myers hotspots.

Several of these areas have been mentioned by
Myers et al. (2000), but their inclusion in the Myers
hotspots was uncertain due to poor data availability.
These data are now available and strongly support
2002). Moreover,
some of the sites have been identified as major gaps
in the network of protected areas (IUCN categories
I-VI plus forest reserves) for threatened and

inclusion (see also Brooks et al..

stricted-range Afrotropical plants (Burgess et al., in
press). This emphasizes the urgency to consider
them in large-scale conservation assessments.

In the Myers hotspots analysis zoological diver-
(Myers et al.,
2000). Patterns of plant and zoological diversity are

sity served as "backup support"
not necessarily congruent. There are, for example,
obvious differences in the importance of the West-
ern Cape or Kaokoveld in the diversity of restrict-
ed-range plants compared to birds or mammals.
Nonetheless, the majority of cells now included in
the redefined hotspots are centers of species rich-
ness and endemism for animals as well. This is true
for the Albertine Rift (Plumptre et al., 2003) in-
cluding the Kivu area, the southwestern connection
of the Eastern Arc to the Mbeya Range, nearly all
of the Afromontane areas mentioned above, includ-
ing Mt. Elgon, Mt. Kenya, and the Chimanimani
Mts., areas in northeastern Southern
Africa and also Katanga (Burgess et al., 2004; Cot-
terill, in press). Range-size rarity patterns for mam-
mals, snakes, and amphibians (Brooks et al., 2001
are very similar. In analyses that are currently most

some of the

—

comprehensive for sub-Saharan zoological diversity,
many of these areas have been classified as irre-
placeable in the context of biodiversity conserva-
tion (Balmford et al., 2001) but are inadequately
protected (De Klerk et al., 2004; Fjeldsá et al..
2004; Burgess et al., press; Rodrigues et al.,
2004). If we want to base hotspots on this list of

a

taxa, many of the newly redefined hotspots would
certainly have an equal priority in comparison to
the areas currently included in the Myers hotspots.

The most obvious difference between the Myers
hotspots and the redefined hotspots is their spatial
resolution, in particular for the Afrotropical region.
The distribution of the species within the Myers
hotspots was not known, but in our study it was
possible to optimize the performance of the rede-
fined hotspots on a spatial scale of one degree.
Hence, several cells within the hotspots have been
replaced by others previously not considered.

The low resolution of inventory-based data limits
not only the spatial precision of the identification
of centers of diversity, but also their comparability.
The Myers hotspots by definition have to include
This
does not take into account the fact that some areas

at least 1500 endemic species per hotspot.

with high regional concentrations of restricted-
range species, such as the Albertine Rift, cannot
match this threshold because they are too small
Plumptre et al., 2003). Since the distribution of
the endemies within the Myers hotspots was not

—

known in many cases, priority of hotspots was de-
termined by ranking the average number of endem-
ics per standard area. In contrast, taxon-based dis-
tribution data can be used to compare any of the
1713 sub-Saharan one-degree cells enabling com-
parison of areas such as the central part of the Al-
bertine Rift or the
demism with parts (not the average) of the hotspots

Maputaland Center of plant en-

in West Africa. In addition, instead of only consid-
ering the number of endemics and the threat per
area, taxon-based data can provide a variety of ad-
ditional parameters, such as diversity at higher tax-
level

onomic or even phylogenetic diversity, en-

abling creation of a hierarchy of priorities.

TOWARD A NETWORK OF
CONSERVATION

PRIORITY AREAS FOR

The Myers hotspots had a very important impact
as a pioneering study demarcating areas where on-
(Mvers, 1990) make it
most urgent to conserve biodiversity. In parallel,

going "mass extinctions”
they have been promoted also as a network of areas
suitable to “protect the most species per dollar in-
vested” (Myers et al., 2000).

seems to be contradictory since the most problem-

At first glance this

atic areas for conservation are unlikely to be those
where conservation is most cost-effective. However,
our results indicate that there are indeed often no
alternatives to protection of narrowly endemic spe-
cies within centers of human settlement and inten-
The 125

sive land use. cells identified as redefined

Volume 91, Number 4
2004

Kuper et al. 533

Africa’s Biodiversity Hotspots

hotspots are inhabited by more than 80 million peo-
ple (population data according to [RWPE], 2002)
and the vast majority of the areas of high plant
endemism in sub-Saharan Africa are characterized
by a very high human footprint (Fig. 1). Despite
their vicinity to metropolitan areas such as Cape
Town, Abidjan, Douala, and Dar es Salaam, and
despite being often completely surrounded by con-
verted land, many sites of “remaining primary veg-
etation” (Myers et al., 2000) within hotspots (such

. for example, Tar and Banco National Park of
Cote D'Ivoire, Table Mountain National Park of the
Republic of South Africa, and the Coastal Forests
of eastern Africa) are irreplaceable due to the many
restricted range species they contain. Due to this
irreplaceability, a large proportion of the areas de-
lineated in the Mvers hotspots cannot be substitut-
ed for other areas, even if the latter had an even
higher plant species richness. In our study, the re-
defined hotspots were constrained by being the
same spatial size as the Myers hotspots. Conse-
quently, the inclusion of new areas formerly not
considered in Myers hotspots resulted in omitting
others previously included. Moreover, a range of
additional areas could not be included despite hav-
ing considerable numbers of restricted-range spe-
cies and despite being highly threatened. For ef-
fective all
containing clusters of strict endemics is a minimum

conservation, inclusion of areas
requirement. For example, the Namib desert and
arid woodlands of northeastern Somalia are also key
areas for plant conservation. Moreover, in order to
translate the hotspots concept to conservation in the
field, floristic checklists of areas with comparatively
intact vegetation and, in particular, checklists of
order to

—

existing protected areas are needed ii
quantify how many restricted-range taxa are al-
ready protected so that conservation gaps can be
determined. This will help African countries com-
ply with international agreements such as the Glob-
al Strategy for Plant Conservation (GSPC), which
requires signatories of the Convention on Biological
Diversity to assure protection of 50% of the most
important plant areas by the year 2010 (Lovett, in

ress
Although many irreplaceable parts of sub-Sahar-
an hotspots are in sites of high pressure for alter-
native land uses, there are also areas with high
range-size rarity and a comparatively low human
impact (Fig. 1). These areas could contribute to op-
efficiency and alleviating
conservation conflicts. However, the data on which
the Myers hotspots and the extremely broadly de-
fined “high biodiversity wilderness” (Mittermeier et
al., 2003) areas are based do not account for com-

timizing conservation

plementarity and hence cannot be used to generate
priorities on the basis of cost-effectiveness. To meet
targets of initiatives such as the GSPC, taxon-based
data are the key information. This includes infor-
mation on species distributions in areas that have
so far remained comparatively untransformed be-
and that tend to be un-

cause of difficult access
dercollected for the same reason. For example. how
many species in the heavily transformed hotspot
around Monrovia could be efficiently protected. in
the largely underexplored Krahn Bassa National
Forest or Sapo National Park in southeastern. Li-
beria? Similarly, we do not yet know the potential
of the undercollected border triangle of Cameroon,
the Republic of Congo, and the Central African Re-
public for the conservation of the lower Guinea rain

forest and its ecotones.

PRIORITIES FOR A GLOBAL
CONSERVATION STRATEGY

We see three priorities for the future application
of taxon-based data in the context of biodiversity
conservation. The first priority must be to acquire
these data at a finer spatial resolution. If the current
progress of data acquisition continues, it is likely
that before 2010 reliable
plants will be available at a quarter-degree reso-
lution for the majority of the globally most biodiv-

distribution data for

erse ecoregions, a scale which approaches that at
which actual conservation actions are implemented.
In particular, in addition to further exploration of
the hotspots, we urgently need better information
on the biodiversity of remote areas with intact veg-
etation and of existing protected areas. А second
priority is to combine botanical and zoological in-
formation to obtain a clear picture of overall bio-
diversity. There is some preliminary evidence of
concordant centers of endemism among many dif-
ferent taxa particularly in geodiverse areas such as
Afrotropical mountains, and these areas should
have a high priority for conservation action. Third,
the high resolution biological data need to be com-
pared with socioeconomic information and remote
sensing data on habitat status. Inevitably, biodiver-
sity in large parts of the redefined hotspots has al-
ready been drastically reduced. The combination of
remote sensing and taxon-based biodiversity data,
therefore, seems to be a promising avenue leading
to identification of those sites where we can protect
biodiversity in an efficient and sustainable way.

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Annals of the
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Esti es and Projections.
J

A REVISION OF THE David Н. Lorence? and Germinal
MASCARENE SPECIES OF a
ELAPHOGLOSSUM

(ELAPHOGLOSSACEAE)!

ABSTRACT

A taxonomic revision of m in the Mascarene Islands (southwest Indian Ocean) is presented here based
on a treatment written for the Flore des Mascareignes. Seventeen spec ies are recognized for the islands of Mauritius
id Réunion. Of these species, seven are endemic. The non-endemic species also occur in Madagase ar, Africa, or the
Pale кар. in general. In addition, five natural interspecific hybrids (nothospecies) occur in the Mascarenes. Two
lectotypes are 5 for the name Acrostichum inversum and are referred pro parte to H. acrostichoides and H.
angulatum.

RÉSUMÉ

Une révision taxinomique d'Elaphoglossum des iles Mascareignes (sud-ouest de l'Océan Indien) est présentée ici,
fondée sur un traitement écrit pour la Flore des Mascareignes. Dix-sept espèces dont sept endémiques sont reconnues
8 | | | |
pour les iles de Maurice et de La Réunion. Les еѕрёсеѕ non-endémiques se trouvent également à Madagascar, en
Afrique, ou dans les Paléotropiques en général. De plus, cing hybrides interspécifiques naturels (notho-espece) sont
8 à |

présents dans les Mascareignes. Deux ee sont désignés pour le nom Acrostichum inversum et sont attribués pro
parte à H. acrostichoides and E. angulatur

ey words: 3 3 hybrids, Mascarene Islands, Mauritius, nothospecies, pteridophytes,
Réunion, sea Nr 11 Ocean.

The Mascarenes are a trio of volcanic oceanic ber (Lorence, 1985). Except in coastal areas with
islands situated in the southwest Indian Ocean. Ар- coral sand, Mascarene soils are derived from de-
proximate sizes and ages (millions of years) of the composed basaltic lavas.
islands are: Réunion, 2500 km, 3.0 MA; Mauritius, Relative to their small surface area the Mascar-

1865 km’, 7.8 MA: and Rodrigues, 110 km”, 1.5 enes possess a diverse pteridophyte flora, with 273
8 | | pm
MA (Fisher et al., 1967; McDougall & Chamalaun, Species comprising 282 taxa including infraspecies
B | 8 B
1969: McDougall et al., 1965). The mean annual Badré € Cadet, 1978; Lorence, 1976b, 1978.
O

precipitation ranges from 1000 to 6000 mm in 1992). Of these, 265 species are indigenous and 8

Mauritius and Réunion and from 1100 to 1700 mm are adventive or naturalized, Of the indigenous spe-
| Rodrigues. The rainy, austral summer season cies, 22.7% are endemic to the Mascarene archi-

11 1 a by occasional tropical cyclones lasts pelago or to a single island.

from December to April, and the relatively drier Among the most species-rich fern genera on the
and cooler winter season lasts from May to Novem- island is Elaphoglossum Schott ex J. Sm., a large

' Use of facilities and financial assistance provided by the Mauritius Sugar Industry Research Institute at Réduit,
auritius, are gratefully acknowledged while the first author served as a U.S. Peace Corps Volunteer at the Mauritius
Herbarium (MAU). A ae of the fieldwork by ше second a was supported by the “PPF Populations fractionnées

et insulaires de l'Ecole di des Hautes Etudes.” We the c а of the following herbaria for making their
specimens available for study: B, BM, К, MAU, MO, 1 р, PR. PRC, PTBG, and REU. Frédéric Badré (P) provided
encouragement and reviewed an earlier version of the manuse ript. We > are grateful to Brigitte Zimmer (В) for о

digital images of the collections in the Willdenow He um (B-W) and for helpful suggestions and comments
thank Victoria Hollowell, John Mickel, Robbin Moran, and Henk van der Werff whose comments and reviews оит
improved the quality of the paper.

? National Tropical Botanical Garden, 3530 pels Road, Kalaheo, Hawaii 96741, U.S.A. lorence@ntbg.org.

' Départe ment Systématique et Evolution USM 0602, Herbier Plantes Vasculaires, Muséum National d'Histoire Na-
turelle, 57 rue Cuvier, 75231 Paris, France. a fr,

à Equipe Classification, E иш et Biosystématique (КА 3496), UMR 5143, Université Pierre et Marie Curie, 12

rue Cuvier, 75005 Paris, Franc

ANN. MISSOURI Bor. GARD. 91: 536-565. 2004.

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

and taxonomically complex pantropical genus.
Worldwide, the genus comprises about 600 species
of primarily epiphytic, lithophytic, and casually ter-
restrial ferns concentrated in tropical wet forests
and cloud forests (Mabberley, 1997; Mickel & Ate-
1980: Mickel & Beitel, 1988). Although the

hortúa.

greatest species diversity occurs in the Andes of

South America,

slight adaptive radiation in a number of oceanic

Elaphoglossum has undergone

islands and archipelagos such as Hawaii with 9
species (Palmer, 2003) and the Mascarene Islands
with 17 species (Lorence, 1978, 1984). In the Mas-
carenes, Elaphoglossum occurs only on the two
largest and highest islands, Mauritius and Réunion:
it is absent from the smaller and drier Rodrigues
Island (Lorence. 1976b). Of the 17 Mascarene spe-
cies, 7 are endemic and 10 occur elsewhere pri-
Africa,

or the Paleotropics in general. In addition to these

marily in Madagascar, the Comoro Islands.

17 species. five natural hybrids (nothospecies) are
known, indicating the genus is in an active state of
evolution in the Mascarenes (Lorence. 1984).

The following revision of Elaphoglossum is based
on a treatment of Lomariopsidaceae s.l. originally
written in French for the Flore des Mascareignes. a
joint collaborative project between the Royal Bo-
tanic Gardens Kew, the Mauritius Herbarium at the
Mauritius Sugar Industry Research Institute. and
Institut de Recherche pour le Développement (IRD.
formerly ORSTOM) based at the Paris Muséum Na-
tional d'Histoire Naturelle. Because publication of
the pteridophyte fascicles for this project has not
yet taken place. we decided to publish this revision
to make the information available in a timely man-
ner. In. addition, we provide supplemental habit
photos and drawings of rhizome scales to facilitate
identification.

MATERIALS AND METHODS

This taxonomic revision is based on 717 herbar-
ium specimens and field observations of all the
Elaphoglossum species occurring in the Mascare-
nes. All measurements given in the descriptions
have been taken from dried herbarium specimens.
Unacetolized spores were mounted in glycerine jel-
ly, and their size measurements were taken exclud-
ing the perispore. Secondary or lateral veins that
are apically free versus united provide an impor-
tant, species-specific character, but the fronds must
be held up to a bright light or, in some cases, chem-
ically cleared to see the venation. Collections with
morphological characters intermediate between two
species that occur in the same vicinity and have a
high percentage of aborted spores (features such as

collapsed, irregular spore shape and size) are sug-
gestive of hybrid origin as already documented for
other pteridophyte genera (Wagner & Chen, 1965:
Wagner et al., 6). Nevertheless, aborted spores
alone are not an absolute criterion of hybridism be-
cause there are several other possible sources of
abortion such as the metabolic conditions of the
plant, which may be influenced by cold or drought
shocks during spore development (Hennipman.
1977).
TAXONOMIC HISTORY

The name Elaphoglossum was first. published,
without description, by Schott (1834), and was not
validated until Smith (1841) attributed the name to
Schott and published a description and cited a type
species. Morton (1965) proposed Elaphoglossum
Schott ex J. Sm.
against Peltapteris Link, which was also published
1 1841.

Elaphoglossum is characterized by its dimorphic

as a conserved generic name

fronds with acrostichoid sori (in addition, nearly all
the species have an elongated ventral meristele in
the rhizome, simple and entire laminae, and free
veins). Because of its soral condition, many species
of Elaphoglossum were originally described under
Acrostichum L. (e.g., Bojer, 1837; Fée, 1845; Baker.
877: Cordemoy, 1895). This proved to be a poly-
phyletic grouping, as the type species Acrostichum
aureum lL.. which also has acrostichoid sori, be-
longs to the Pteridaceae (e.g.. Tryon & Tryon.
1962). Most taxa of Elaphoglossum originally de-
scribed in Acrostichum were subsequently trans-
C. Presl

or Hymenodium Fée (now both considered syno-

ferred to Elaphoglossum, or to Aconiopteris

nyms of Elaphoglossum). Most of these transfers
were made by Moore (1857-1862).

The difficulties in establishing phylogenetic. re

lationships of Elaphoglossum to other ferns may ex-
plain why in modern times the genus has been tax-
onomically treated along diverse lines, namely: (1)
as a part of the family of Lomariopsidaceae Alston
(Alston, 1956; Kramer et al., 1990; Moran & Riba,
1995). which is the concept retained within African
literature (e.g., Alston, 1959; Tardieu-Blot, 1959,
1960; Schelpe, 1969; Roux, 2001; Mickel, 2002):

(2) as a member of the family Elaphoglossaceac
described by Pichi Sermolli (1968); (3) as a mem-
ber of a subfamily: Aspleniaceae Mett. ex A. B.

Frank subfam. Elaphoglossoideae (Pic. Serm.)
Crabbe, Jermy € Mickel (Crabbe et al.. 1975): and
(4) as a member of the tribe Bolbitideae Pic. Serm.
Herter

included in the family Dryopteridaceae

(Tryon & Tryon, 1982).

538

Annals of the
Missouri Botanical Garden

The most recent comprehensive systematic ac-
count of the genus as a whole is the Monographie
des Genus Elaphoglossum (Christ, 1899). This treat-
ment covered 134 species and detailed 32 taxo-
nomic groups. More recently Mickel and Atehortúa
(1980:
subsections, but they emphasized that

41) subdivided the genus into sections and
"this treat-
ment is provisional because a complete under-
standing of the genus can be had only after the
species are better known." Even with the first phy-
logenetic studies of the genus (Rouhan et al.,
2004), knowledge of the systematics and phylogeny
of Elaphoglossum is far from complete, and new
species continue to be described. The present pa-
per aims at providing new knowledge and a modern
taxonomic treatment of the genus in the Mascarene
region.
TAXONOMIC TREATMENT

J. Bot. (Hook.)

el typ. cons.

Elaphoglossum Schott ex J. Sm.,
A(27): 148. Aug. 1841,
TYPE: Elaphoglossum conforme (Sv.) J. Sm..
J. Bot. (Hook.) 4(27): 148. 1841 [Acrostichum

Syn. Fil. (Sw.) 10, 192. 1806].

nomi.

conforme Sw.,

Fée. Мет. Foug., 2: 20. 1844 [1845].
pire crinitum (L.) Fée, Мет. Foug.,
2: 90. 1844 15] [Acrostichum crinitum L., Sp. 1
1068. eh
Peltapteris L ink, Fil. Spec. 147. 1
17 7 (Su.) С.
d peltata Sw..
зира C. sl, Abh. . 6
ser. 5, 1851. : Mic oup 5
furcata een] C. Presl, Epimel. p 19 [Os-
munda bifurcata Jacq.. ica P z 2. tab.
20(4). 1789]

Hymenodium
TYPE:

—

. TYPE: Pe wears

1

< 2

The following discussion clarifies the nomencla-
ture and the typification of the genus Elaphoglos-
sum. H. W. Schott was the first to propose the name
3. 1834). but

this name lacks a description and consequently was

Elaphoglossum (Gen. Fil.: 30, tab.
not validly published. Validly publishing Elapho-
glossum, J. Smith attributed the name to Schott (J.
Bot. 4(27): 148. 1841) and referred six species to
the genus, but he did not select one of them as the
125.

1875), J. Smith clearly chose E. conforme as the

type. In a subsequent publication (Hist. Fil.:

types Since the date of publication of Elaphoglos-
sum is 1841 and not 1834,
in 1836, should have priority

Aconiopteris, which was
validly published
over Elaphoglossum when these genera are united.
In order to avoid replacing the well-known generic
name Elaphoglossum by Aconiopteris. the name
Elaphoglossum and its type E. conforme (Su.) J. Sm.
are conserved respectively as nomina conservanda

and typus conservandus (ICBN, App. ША; Voss et
al., 1983: 296) against Aconiopteris, which is based
on a type different from that of the conserved name
ра Art. 14.4) аз follows:
„ Presl. [Tent. Pterid.] in Abh. Kónigl. Böhm. Ges.
10(17). 1836 (ante 2
Aconiopteris subdiaphana (Hook. &
Tent. Pterid. 236, tab. 10(17). 1836
|Acrostichum subdiaphanum Hook. & Grev.. Icon.
ilic. 2. tab. 205. 1831].
Small to medium-sized epiphytic, epilithic, or

Aconiopteris

A

ur ser, 4, 5: 236, tab.
De C.). TY PE:

C. Presl.

occasionally terrestrial ferns; rhizome short- to
long-creeping, branching or not, dictyostelic, dor-
siventral or radial, fronds in 2 or 3 to 5 ranks (Mas-
carene species), paleaceous, scales basifixed.
Fronds simple (all Mascarene taxa), very rarely fla-
bellately lobed, with stipe jointed and swollen into
a persistent, dark phyllopodium bearing small lat-
eral aerenchymatous outgrowths when young: blade
simple, entire, usually erect but sometimes pen-
dent, chartaceous to coriaceous, glabrate to densely
paleaceous, scales often deciduous; secondary (lat-

eral

—

venation pinnate, simple or dichotomous, tips
apically free and thickened or uniting into a sub-
marginal vein or commissure, rarely branching and
anastomosing reticulately (not in Mascarene taxa),
margin often revolute. Fertile frond similar in shape
to. sterile, but blade usually smaller and longer
stiped; sporangia densely covering abaxial surface
of blade except along costa and margin. Spores
bilateral, reniform, exine

monolete, elliptic to

smooth, perispore granular to spiny forming folds

—

ır crests. Gametophyte subcordate or ribbon-like,
margins undulate or crisped and bearing unicellu-
lar hairs with waxy tips, rhizoids reddish brown.
Chromosome number 41 (Manton & Sledge,
1954).

The generic name Elaphoglossum refers to the
tongue-like shape of the laminae (from the Greek

words elaphos = stag, and glossa = tongue).

In the Mascarene Islands most species grow as
low to high epiphytes or are casually terrestrial in
moist and wet forests and ericoid (heath) forma-
tions. Where conditions are satisfactory, the plants
usually root in mats of bryophytes on trees, at bases
of shrubs and trees, or on mossy logs or boulders.
One species, E. lanatum, is restricted to soil
rock of shady stream banks and cliff faces, and E.
spatulatum grows specifically on large boulders in
stream beds.

The Mascarenes harbor seven endemic Elapho-
glossum species. This suggests the genus is ac-
tively evolving in this archipelago (Lorence,
1984), especially given the relatively recent emer-
five natural

gence of these islands. Furthermore,

Volume 91, Number 4 Lorence & Rouhan 539
2004 Mascarene Elaphoglossum

hybrids occur in the Mascarenes (see Lorence. plications of the occurrence of these hybrids
1984. for detailed discussion concerning the im- the Mascarenes).

KEY TO THE MASCARENE SPECIES OF ELAPHOGLOSSUM

la. Ste d blades glabrous or bearing (at least when voung) rare to scattered, minute. енн scales 0.5 mm
or less long with margins beating short multicellular hairs with bulbous, glandu lar tip
ш Sterile blades broadly élliptic to ovate, usually 3 em wide or broader
3a. Rhizome scales, filiform or bristle- like, dark reddish brown or blac
1

Rhizome scales 3-5 mm 1 2 suff, shiny, black; veins in m apically free and in part
uniting intramarginally at lips . 14. E. Xr ugha

Ib Hos scales 8-20 mm [uh fle ible dull. brown to black: veins uniting apically into a
ibmarginal commissure 0000000000 — 18. E. sieberi

w

. Albina scales broadly ovate to lance 'olate. pale orange- -brown or tan

53 пхоте scales broadly ovate, the base auriculate with кед lobes: rhizome long-

A ee ee Bt 2 eua
Rhizome se miles narrowly ovate to oblong; lac king « overlapping База! lobes: yita short-
creeping,

5h.

6a. ame scales 4-10 mm long. 1-1.5 mm wide, curling, with margins involute and
bearing long. gland-tipped projections. these more numerous toward 15 bi ч veins
free al lips oi aint
ob. Rhizome se salen | 10— П 5-25 mm long, 2-3 mm йв, fli at, “with margins entire or be
ing rare short projections: veins uniting apically into submarginal commissure
жишш А 18. Е. sicatoncdinm
2b. Sterile blades narrowly йү, pne Or linea ar, изиг alls less hats 3 em wide.
7a. Surfaces of sterile blade bearing scattered, persistent, light brown resinous punctations (seen
under magnification, but not visible on al adult specimens): veins uniting apically d a sub-
marginal commissure — . E. richardii

Tb. Surfaces of sterile blade leo king n resinous punctations: veins free apically
a. Rhizome scales thick, « hub brown to black, opaque except id basally.

9a. Sterile frond with blade at least 15 em long — 6. Е. coursú
9b. Sterile frond with blade 6-14 em lon 5. Е. Xcadetiü

8b. Rhizome scales thin, papery, pale to ыы brown, translucent or sometimes opaque api-
cally.

10a. Rhizome scales with darker bands toward apex
10b. Rhizome scales uniformly pale golden or reddish brown.
а

. E. acrostichoides

mÓT

Rhizome long-creeping. often branching: fronds spaced 1.5 em or more apart:

rhizome scales flat, broadly ovate, entire .. 3. V. 5
IIb. 5 short- to moderately long-c reeping, rarely branched; fronds spaced
em or less apart: rhizome sc de crisped, involute, narrowly ovate E linear-
99 margins ciliate especially b: кеу тех 12. E. lepe reanchet

~

Sterile blades bearing (at least when young) on both surfaces and/or the margins numerous conspicuous
scales, either subulate, laminate, peltate, or substellate
12а. Scales of sterile frond stellate or substellate. vid. 1 to 8 straight hair teeth 11. V. lancifolium
12b. Scales of sterile blade basifixed or peltate. or subulate.
13a. Se ales. of sterile blade subulate. margins entire or occasionally minutely ciliate apic SHE
ile

14a. Scales of sterile blade dark brown. confined to margins and costa ‚К. hybridum
14b. Scales of sterile blade pale brown to reddish brown. scattered over both n of th«
blade.

15a. Sterile bk pu linear, thinly chartaceous and translucent, veins readily visible whe n

veld up to light . aubertii
150. Sterile blades elliptic, narrowly obovate, or spatulate, thickly chartaceous. veins not

visible when held up to light.

Іба. Sterile blades TS to а obovate, 1.5-5.5 X 0.5-1.2 cm. apex obtuse

— —— y 10. F. spatulatum

6b. Sterile blades e lliptic, 7 10 x 1.52 cm, apex acute — 17. E. Xsetaceum
13b. Scales of sterile blade peltate or Vii e d flat central portion, the margins fimbriate or

strongly ciliate

Іта. Scales af sterile blade closely appressed, suborbicular, scarious, densely fimbriate: rhizome
scales with margins scarious or fimbriate.

18:

Rhizome seales 2-3 mm long, claw-like, opaque. dull brawn with арна margins:
sterile blade with veins all uniting apically into a submarginal commissur

ds - 22. E tomentosum
18b. Risas scales 6-12 mm long. кты with losa: БЫ аға apex, shiny cas-
taneous to black with pale scarious margins: sterile blade with veins free (some uniting
apically in H. vident anis bium).

540

Annals of the
Missouri Botanical Garden

19а. Sterile blade with veins free apic cally with thickened tips; rhizome sc cales black
7. E.

with scarious „ nl margins

19b. Ste ile blade with

heterolepis

veins uniting apically into submarginal loops, йы \охаг‹

base and apex of blade free with thicke ned tips; rhizome scales 5 with

sparsely dentate or glandular- ciliate margins

^^
ео

x heterophlebium
h

17b. Scales of ste nile blade spreading, toothed with RE paired hair teeth; 1 scales wit
margins bearing (at least bas: ally) short hair teeth or sessile glands.
20a. uns blades paleaceous only on adaxial surface, rarely a few se ales а or

surface along costa

aba
20b. Ste ile 3 's paleaceous on both pui es, al least when young.
d on rhizome, not densely caes

2la. Fronds 2-ranke

1
7. stipitatum

pitose; steri ile blade covered when

young with E matted scales bearing long. tangle d marginal cilia, the scales

soon dec iduou

Scales on TN surface of sterile blade forming a loose tomentum

tomentum

10. E. lanatum

22b. S Wales on adaxial ү e of sterile blade c dose ly appressed 1 a thin
. E.

2 Xadulterinum
th

21b. Fronds 2- to 5- ranked on rhizome, usually densely caespitose; ste ae Th wil
|

23a. Sterile blade with both surfaces obscured by a

marginal long hair teeth.
layer of reddish dodo

se n with dark brown to black scales often present along abaxial surf

`

E. ae dn

E:

of «
23b. Ste ie blade with both surdse es visible, covered with loose, pal reddish

brown scales along the veins

1. Elaphoglossum acrostichoides (Hook. «
Grev.) Schelpe, J. S. African Bot. 30: 190.
1964. Hook. & Grev.,
Icon. Filic. 2: tab. 186. 1830. Drymoglossum
ac a е 1 & Grev.) T. Moore, Index
Fil.: 3 TYPE: South Africa.
Good TE D. Thom s.n. Hb. Hook] (holo-
type, K!). Figure ТА.

Vittaria acrostichoides

аи falcatum (Fée) T. Moore, Index Fil.: <“

5 Е atum Fée, Мет. Foug.,

ab. 210. 844 [1845]. TYPE: ои [Réunion]
ыз a. & Richard s.n. [Hb. Bor
27,49] (holotype, P).

Ёш ин inversum (C ordem.) H. Christ,

Denkschr. Allg.

Neue

Gesammten Natur-

wiss. 36(1): 146. 1899, Acrostichum inversum Cor-
dem., Fl. Réunion, part 1: 84. 1891. TYPE: Ré-
union. Grande Montée de la Plaine des Cafres, 1899,
E. J. de Cordemoy s.n. pro parte, 2 right-hand spec-

imens only (lectotype, designated here, P!).

Fronds moderately spaced 0.8-1.5 em distant,
borne in 2 ranks; rhizome long-creeping, 2—4 mm
diam., occasionally branching, densely paleaceous:
scales 3-5 1.2-1.6 mm, ovate to ovate-elliptic,
brown with dark brown bands at base and apex (or
often almost completely dark and only margins
clearer), very often lustrous, base truncate, cordate,
or auriculate, acuminate,

apex margins entire or

bearing toward base short teeth or bulbous-tipped
cilia, cells small, rectangular. Phyllopodia to 6-10
mm long, slightly swollen, brown to dark brown, pa-

eaceous; sterile fronds 10—25(—11) cm: stipe 3-12
em, canaliculate, narrowly winged distally, brown to

blackish, bearing scattered caducous scales like

Cape of

». E. rufidulum

those of rhizome: blade narrowly elliptic to oblong,
often somewhat falcate, 7—16(-26) X 0.7-2(-3) ст,
base narrowly cuneate to attenuate, apex acute to
long-acuminate, coriaceous to subcoriaceous, costa
canaliculate adaxi-
ally, margins revolute, veins distinct to somewhat in-

prominulous, rounded abaxially.

distinct, free with thickened tips, adaxial surface of
blade glabrate, abaxial surface of blade bearing scat-
tered, brown, ovate scales 3—4 X 2 mm with margins
dentate to ciliate mixed with smaller substellate
scales with glandular marginal cilia. Fertile frond 9—
26(—40) em long; stipe slender, about half total frond
length; blade 6-16(-25) em, narrowly elliptic, fal-
cate, base narrowly cuneate, decurrent, apex acute.
Spores 35—40 X 20-25 um (excluding perispore),
perispore cristate, crests 3-6 um high, with entire
to finely sinuate margins.
Distribution and habitat. Réunion; also known
from Madagascar, the Comoro Islands, tropical and
southern Africa, Sao Tomé, and Fernando Po. In Ré-
union E. acrostichoides occurs from 1200 to 2300 m
in moist and wet forests and ericoid formations as
an epiphyte and saxicolous on mossy rocks.
acrostichoides

Jiscussion. Elaphoglossum

greatly resembles E. coursii by its general appear-
ance, but differs by paler, less stiff rhizome scales.
Elaphoglossum acrostichoides resembles E. angu-
latum by the long-creeping rhizome, but differs by
less widely spaced fronds. Elaphoglossum acrosti-
choides can be distinguished from the other species
in the Mascarenes by non-appressed, dark-streaked
rhizome and stipe scales. In Réunion it hybridizes
with E. coursii (Lorence, 1984), forming E. саден

Volume 91, Number 4 Lorence & Rouhan
4 Mascarene Elaphoglossum

Figure l. Habit of some Mascarene Elaphoglossum баж cies. All the И show specimens with sterile and
B. The long- -C reeping rhizome of E.
р,

ае fronds. —A. E.
angulatum from pre? жу in 216. —
Réunion, Rouhan et al. 2 . E. sieberi гени Mauritius, Brise

acrostichoides from Réunion, Rouhan & uga?
C. richardii "from Réunion, € et al.

Fer Reserve. Scale bar

aubertii. from

rs — 2 cm.

542

Annals of the
Missouri Botanical Garden

Lorence. Elaphoglossum acrostichoides resembles
E. glabellum J. Sm. from the Neotropics in nearly
all characters; certain specimens of E. acrostichoi-
des are indistinguishable from the Neotropical ones
(Moran & Smith, 2001). We found in the Paris her-
barium only one sheet bearing the name Acrosti-
chum inversum along with the annotations “La Ré-
union" and “Jacob de Cordemoy,” and the date
“1899” on the label is subsequent to the original
publication (1891). Of the four specimens included
on this sheet, the two right-hand specimens only
are Elaphoglossum acrostichoides (the two left-hand
remaining specimens being E. angulatum (Blume)
T. Moore), necessitating the need to designate a lec-
totype (ICBN, Art. 9.9; Greuter et al., 2000). We
hereby designate these two right-hand specimens
of E. J. de Cordemoy s.n. as the lectotype of Acros-
tichum inversum Cordem., herein referred to E. ac-
rostichoides (Hook. & Grev.) Schelpe.

Selected ко 8 REUNION. Bébour,
Lorence in MAU 1 3 (MAU); near Riviére des Mar-
souins, Lorence in MAU ipa hus AU); path to Piton de

' 15621 (MAU); Col de Bébour,
RE U): Buca 'an p" лау, inet 801 (P); С
laos, au dessus des Thermes, Cadet 2 (REU); Сапа
и Cadei 805 (P) р pente ш ы Cadet 1929А
(P); sentier GR КІ entre “Le Bloc” et le gite de :: Caverne
e ооң 215 (NY, Р); Cirque de Salazie, Rouhan
et al. 229 (Р, PTBG); Dimitile, Rouhan be б ойыш d 204
Ж Gran Bénard, Pic Matdo, Cadet 1749 (P); Grand Ma-
. Lorence in MAU 15637 (MAU); Пе à Guillaume,
Badré 866 (P); Piton des Neiges, Lorence in MAU 15648
(MAU, MO); sentier de la riviere, Rouhan € Grangaud
PTBG); Plaine des Fougères, Oct. 1850, Boir-
in s.n. (P); Salazie, p oda Mézières s.n. (P); sentier
de Roche Ecrite, Badré s Rs ; St. Paul, i
Alcide, Rouhan et al. 2 NY, P, PTB G); volcan
(Massif a la Fournaise), ET id Bellecombe, Lorence &
Lorence 2520 (MO).

eS

d

Elaphoglossum Xadulterinum Lorence Ha-
phoglossum lanatum (Bojer ex Baker) Lorence
X E. tomentosum (Bory ex Willd.) H. Christ].
Fern Gaz. 12: 347, fig. 4. 1984. TYPE: Maur-
itius. Valley of Cascade 500 Pieds (Cascade
Alexandra). 1974, Н. Lorence 874 (holo-
type, MAU 163009.

Fronds caespitose, spaced 3-5 mm distant,
borne in 2 ranks: rhizome short-creeping, 2-3 mm
diam., rarely branched, densely paleaceous apical-
0.6 mm,
lanceolate, castaneous, opaque, base cordate to au-

ly; scales 4. narrowly ovate to
riculate, entire or bearing clear, globose marginal
glands, apex narrowly acuminate, filiform, sinuate.
margins sparsely glandular dentate-ciliate, cells
opaque. Phyllopodia 6-8 mm long, thickened, dark
brown, paleaceous basally; sterile fronds (27-)35—

)10-15 em, 0.5-1 mm diam.,

stramineous, canaliculate, bearing scattered, ap-

48.5 cm; stipe (8—

pressed, brown caducous ovate scales 1-2 X 0.5
mm, base obtuse, apex acute, margins scarious,
glandular-ciliate, these intermixed with smaller,
matted scales; blade linear-oblong to linear, (19—)
25-32 X (1.4—)1.8-2.5 cm, base narrowly cuneate,
decurrent, apex acute to acuminate, subcoriaceous,
costa stramineous, prominulous and rounded abax-
ially, shallowly canaliculate adaxially, both surfaces
covered with a homogenous layer of thin, matted,
appressed pale brown to buff-colored, ovate to sub-
1-1.5 X 1
rounded to cordate or sagittate, base and margins

circular scales mm, basifixed, base
bearing long, spreading arachnoid cilia, pedicel
and center darker brown, subtended by cluster of
globose glands, cells hyaline, thin-walled, adaxial
surface of lamina glabrescent, veins unbranched or
bifurcate, in part free apically with tips thickened,
in part uniting submarginally, both of
blade with scattered hair-toothed to deltoid scales

surfaces

^

0.2-0.5 mm long, glandular-ciliate at base. Fertile
frond 20-25 cm long; stipe 10-11.5 cm, 1 mm
11-14

chartaceous, base narrowly cuneate, apex acute,

diam.; blade 0.7-1 cm, linear-elliptic,

—

adaxial surface with dense layer of matted scales
as in sterile frond, margins revolute. Spores 82%
aborted, normal spores 35-38 X 25-27 um (ex-
cluding perispore), perispore cristate, crests low,
1.5-3 mm high, sinuate to finely erose-dentate.

Distribution and habitat. Elaphoglossum Xad-
ulterinum is known only from the type locality in
Mauritius at the southern extremity of the central
plateau, altitude 600 m. The hybrid occurs on boul-
ders below cliffs in wet forests where the parental
species E. lanatum and Е. tomentosum occur near-
by (Lorence, 1984).

Discussion. Elaphoglossum Xadulterinum re-
sembles E. tomentosum in its habitat preference

epiphytic or epipetric), erect fronds, and sterile

—

blade shape, although its rhizome scales are glan-
The hy-

brid’s mixed venation, in part free as in E. lanatum

dular and resiniferous as in E. lanatum.

and in part uniting intramarginally as in E. tomen-
tosum, and intermediate frond scale morphology
distinguish it from the parents.

Specimens examined. MAURITIUS. Valley of Cascade
500 Pieds (Cascade Alexandra), Lorence sub MAU 16307
(MAU, M. Lorem 1609 (MO), Lorence 1610 (MO), Lor-
ence 647 (MAU).

3. Elaphoglossum 5 (Blume) J. Moore.
Index Fil: 5. 1857. J angulutum
Blume, Enum. Pl. Javae 101. 1828; Fl. Javae

Volume 91, Number 4
2004

Lorence & Rouhan 543

Mascarene Elaphoglossum

3: 25 (1828), tab. 6 exhibiting a drawing of the
type specimen. Olfersia pu (Blume) С.

Presl, Tent. Pterid. 234. 18 "Y PE: Java. C.
L. von Blume s.n. (аот a Figure 1B.
Syst. 15:

Md ши: alstonii Tardieu, Notul. 133.
ene laurifolium Fée, Mém. Foug.. 2:
A tab. 7. 1 4 [1845], non Acrostichum ae
Thouars, inn Fl. Tristan d'Acugna: 31.
TYPE: Bourbon [Réunion]. 1840, leat us
deres 14 [Hb. Bory 27,15] (holotype, P!).
Elaphoglossum inversum (Cordem.) Н. ser Neue
Denkschr. Allg. Schweiz. Ges. Gesammten Natur-
36(1): 146. 1899. 3 inversum Cor-
dem., Fl. Réunion, part 1: 84. 1891. TYPE: Ré-
union. Grande montée de la P -— des Cafres, 1899,
E. J. de Cordemoy s.n. pro . 2 left- ll speci-
mens only (lectotype, piede here.

>

WISS.

Fronds widely spaced 1.5—4 cm distant. erect.
borne in 2 ranks; rhizome always very long-creep-
ing, 2-3 mm diam., occasionally . ‘hing, clothed
with appressed scales; scales 3-5 X 2-3 mm,
ovate, thin, light brown or reddish brown, base au-
riculate with overlapping lobes, apex acute to acu-
minate, margins entire or bearing toward base rare.
short bulbous-tipped cilia, cells squarish. Phyllo-
podia to 15 mm long, slightly swollen, brown to
dark brown, paleaceous; sterile fronds 20-40 cm:
stipe 9-17 cm, canaliculate, brown to orange, bear-
ing scattered spreading, light brown, ovate scales;
blade narrowly elliptic to narrowly ovate, 10-16 X
2—4 cm, base narrowly cuneate, shortly decurrent,
apex acute to acuminate, coriaceous to subcoria-
ceous, costa prominulous, rounded to angled abax-
ially, canaliculate adaxially, margins revolute, veins
often indistinct, in part free apically with thickened
tips and in part uniting into an intramarginal com-
missure, adaxial surface of blade glabrate, abaxial
surface of blade bearing a few scattered, ovate
scales 1-3 mm long. Fertile frond 20-40 cm long;
stipe as in sterile, blade as in sterile but narrower.
Spores 28-30 х 20-23 рт (excluding perispore),
perispore cristate, crests 4-5 um high. with entire
to finely sinuate margins.

Distribution and habitat. Réunion: also Mada-
gascar, tropical Africa, southern India. Sri Lanka.
Java, Sumatra, Borneo, New Guinea, Philippines.
New Caledonia, and Taiwan. In Réu ‘union, Elaphog-
lossum angulatum occurs as an epiphyte or casu-
ally terrestrial in ericoid io from 1300 to
2200 m.
Discussion.
sum acrostichoides by the long-creeping rhizome

This species resembles Elaphoglos-

and general appearance, but differs by more widely
E. angulatum can also be distin-

guished by its ovate, appressed, uniformly colored,

spaced fronds.

light brown or reddish brown rhizome and stipe

scales, by the veins in part uniting into an intra-
marginal commissure, and by the erect fronds (see
Sledge, 1967, for more details).

The type of Acrostichum angulatum is from Java
and was collected by Blume. Carl Ludwig von Blu-
me worked at Leiden (L). and according to Stafleu
and Cowan (1976) all his collections were depos-
ited in L. Nevertheless, many specimens were dis-
tributed from Leiden after his death, and not always
with the regard we now have for type specimens (Р.
Hovenkamp (L). pers. comm.). There is a specimen
of Blume s.n. housed in K and bearing a label
"Herb. Lugd. Batav."
gulatum" written by Blume. Furthermore, this spec-

with the mention “Acrost. an-
imen matches well the drawing of the tvpe speci-
men in Flora Javae. For this
specimen of Blume s.n. housed in K is identified

these reasons,
as the holotype of Acrostichum angulatum Blume.
Concerning the typification of Acrostichum inver-
sum, although the date “1890” written on the label
is posterior to the original publication (1891), we
found in the Paris herbarium only one sheet bear-
ing the name Acrostichum inversum along with the
annotations "La Réunion"
moy.” Of the four specimens included on this sheet.
the two left-hand specimens only are Elaphoglos-
sum angulatum (the two right-hand remaining
specimens are E. acrostichoides), necessitating the
need to designate a lectotype (ICBN, Art. 9.9;
Greuter et al., 2000). We hereby designate these
two left-hand specimens of E. J. de Cordemoy s.n
as the lectotype of Acrostichum inversum Cordem..
here referred to E. angulatum (Blume) T. Moore.

and "Jacob de Corde-

Selected specimens examined. RÉUNION.
near Rivière des Marsouins. Lorence in MA
(MAU, МО); Cilaos, sentier GR RI entre “Le ded
gîte de la Caverne Dufour, е 216 (
pente du Cirque, Cadet 1930 (Р); Plaine i км.

rd., P. О. Wiehe 1721 (MAU); Piton des M Lorence

1 MAU 15612 (MAU), Lorence in Mad 5615 (MAU)
lore 408 (MO); Plaine des Cafr pe 5 la source

reor Cadet 1778 (P); Plaine des Taek Rouhan et
233 (Р); Plaine des Palmistes, la Grande Montée, Ca-
det 504 (P); volcan, Enclos Fouqué, Cadet 1556 (P. top 3
ap iene volcan, Pas de Bellecombe, Rouhan & Gran-

р);

220 (NY,

Bébour.
J 156

gaud 2

4. Elaphoglossum aubertii (Desv.) T. Moore. In-
il.: 5. 1857. Acrostichum aubertii Desv.,
Ges. Naturf. Freunde Berlin Mag. Neuesten
Entdeck. Gesammten Naturk. 5: 309. 1811
TYPE: Bourbon [Réunion]. 1808, A. Du Petit-
Thouars s.n. (holotype. P-JU 992!). Figure 1D.

dex F

Fronds caespitose, borne in 3 ranks: rhizome
very short-creeping, 2-3 diam., rarely
branched, densely paleaceous: scales 6-8 х 0.5—

mm

544 Annals of the

Meret Botanical Garden
| mm, narrowly ovate to oblong, dark reddish апу other species in the genus (Rouhan et al.,
brown, base cordate, apex narrowly acuminate, 2004). Thus, E. aubertii may possibly be conspe-

margins entire, cells fusiform, to very linear for the
marginal cells. Phyllopodia 2-3 mm long, slightly
flattened and constricted, dark brown to black; ster-
ile fronds 10—30 cm; stipe 2-6 cm, 0.5-1 mm
diam., stramineous, canaliculate, bearing scattered
to abundant, reddish brown, narrow, spreading su-
bulate scales 3-5 mm long, 0.25-0.5 mm wide,
base tubular and closed, apex long-acuminate, mar-
gins with short, glandular-tipped cilia basally, en-
tire above; blade linear-oblong, 8-24 X 0.8-1.4
cm, base cuneate to narrowly cuneate, apex acute
to rounded, chartaceous, costa prominulous and
rounded abaxially, shallowly canaliculate adaxially,
both surfaces bearing spreading subulate scales as
in stipe, margins thin, flat, translucent, bearing
fringe of reddish brown, spreading scales as on cos-
ta, veins distinct, unbranched or bifurcate, free api-
cally, tips thickened and dark, both surfaces of
blade with scattered subulate to deltoid scales 0.2—
0.5 mm long, glandular-ciliate at base. Fertile frond
about equaling or slightly shorter than sterile frond;
stipe slender, : to 3 times longer than sterile stipe:
.7-1.4 em, narrowly ovate to narrow-
r rare

blade 3-7 X
ly elliptic, va cuneate to truncate «
subcordate, apex acute, costa sparsely and minute-
ly paleaceous on both surfaces, sporangia lacking

-

on margins and extreme base of blade. Spores 34—

22-25 um (excluding perispore), perispore
surface echinate, spinules 2.5—4 um high.

Distribution and habitat. Réunion: also known

from Madagascar, Comoro Islands, tropical and
southern Africa,
Réunion this species occurs in wet forests and er-
icoid shrubland from 200 to 1500 m elevation.

aubertii on Mauritius is doubtful

Fernando Po, and Sao Tomé. On

The
occurrence of E.
and based on a single specimen (Boivin s.n.), the
type of А. boivinii Mett. ex Kuhn (Filic. Afr. 43.
1868), which has not been located. No other col-
lections are known from Mauritius.

Discussion. Elaphoglossum aubertii can be dis-
tinguished by spreading, subulate scales, conspic-
uous hydathodes, and short petioles (Y to М the
length of the blades).

Elaphoglossum aubertii greatly resembles E. ex-
imium (Mett.) H. Christ, a species of South and
Central America (Moran & Smith, 2001). Both spe-
cies show morphological characters so similar that
distinction is very difficult without knowing the
geographical origin. This close relationship is
strongly supported by phylogenetic analyses based
on molecular data, since E. aubertii and E. eximium
appear more closely related to each other than to

cific with E. eximium (in which case E. aubertii
would have priority).
Selected specimens examined. REUNION. Bébour,

Lorence in MAU 15629 (MAU); Plateau de Bébour, Bosser
21503 (Р); Dimitile, alias & Grangaud 206 (Р); Forét

>, Cadet 123 (Р); Monte tée de la Plaine des Caf-

i à Boue, Plaine des Caf-

759 (P); Plaine de вам res, Rouhan et al.

226 (NY, Р, PTBG); Saint-Philippe, бз. Vallée, Badré

1004 Cr Paul, sentier de l'ilet Alcide, Rouhan et al.
241 (NY, P).

5. Elaphoglossum Xeadetii Lorence [Elapho-
glossum acrostichoides (Hook. & Grev.) Schel-
pe X H. coursii Tardieu], Fern Gaz. 12: 346,
fig. 3. 1984. TYPE: Réunion. Piton de la Four-
naise, Plaine des Sables, T. Cadet 2063 (ho-
lotype, REU!; isotype, P not seen).

Fronds spaced 2—4 mm distant, borne in 2 ranks;
rhizome short-creeping, 2-4 mm diam.,
branching, densely paleaceous; scales 2
mm, ovate, shiny black, base cordate or auriculate,
pale brown, apex acute to acuminate, black and
opaque, margins bearing rare glandular-tipped cilia.
Phyllopodia to 5-7.5 mm long, swollen, dark brown
to black, paleaceous toward base; sterile fronds (6—
38-14 em; stipe (2.2-)3.6—6.5 ст X 0,5—1 mm, can-
aliculate, stramineous, bearing scattered dark brown,
discolorous ovate scales 2-3 X 0.5-1 mm, margins
sparsely ciliate; blade narrowly elliptic, 4-10 X 0.7—
5 em, base narrowly cuneate, narrowly decurrent,

—

apex acute with rounded tip, coriaceous, costa prom-
inulous, rounded abaxially, slightly canaliculate
adaxially, margins revolute, veins indistinct, dichot-
omous, apically free with thickened tips, adaxial sur-
ace of blade glabrate, abaxial surface bearing mi-
5 mm diam., with a

pag)

nute brown, substellate scales 0.5
few larger scales along costa. Fertile frond 14-18.5

=

em long; stipe 7.5-14 em, about three times longer
than sterile stipe; blade 6-8.5 X 0.9-1 cm, narrowly
elliptic, base narrowly cuneate, slightly decurrent,
apex obtuse, costa stramineous, veins indistinct.
Spores ca. 90% aborted.
Distribution and habitat. Réunion, known only
from the type collection. Elaphoglossum Xcadetii
represents a natural hybrid between E. acrostichoides
and H. coursii, which both occur at the type locality
on the Piton de la Fournaise massif, an active vol-
cano (Lorence, 1984). The putative hybrid was col-
lected from fissures in lava at 2300 m among heath
vegetation. A morphologically similar collection from
Mt. Ankaroka, Madagascar (H. Humbert & G. Cours

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

17521, PH. may represent this hybrid, as both pu-
tative parents also occur in Madagascar.

Elaphoglossum Xcadetii resembles E. coursii but
differs by its longer, narrower rhizome scales. short-
er coriaceous sterile fronds with indistinct veins,
and fertile fronds up to twice as long as the sterile
ones.

6. Elaphoglossum coursii Tardieu, Notul. Syst.
15: 434. 1959. TYPE: Madagascar. 1951, H.
Humbert & R. Capuron 24918 (holotype, P!;
isotype, К!).

Fronds moderately spaced 0.5-1 cm distant,
borne in 2 ranks: rhizome moderately long-creep-
ing. 1-3 mm diam., occasionally branching, sparse-
0.4-0.7 mm,
to ovate-elliptic, dark brown to black, paler at base

ly paleaceous: scales 1—1.5 ovate
and margins, opaque, rigid, base auriculate with
overlapping lobes, apex acute, margins with bul-
bous-tipped cilia especially basally, cells square to
fusiform. Phyllopodia 5-10 mm long, slightly swol-
en. brown to blackish, paleaceous: sterile fronds
20-35 cm; stipe 6-15 cm, slender, canaliculate,
stramineous to dark brown, bearing scales like
those of rhizome but larger and paler; blade linear-
elliptic to linear, 10-24 X 0.6-1.8 cm,
rowly acute, attenuate and decurrent, apex acute to

base nar-

long-acuminate, subcoriaceous to coriaceous, costa
prominulous and rounded to angulate abaxially.
canaliculate adaxially, margins strongly revolute.
veins distinct to somewhat indistinct, often bifur-
cate, apically free, adaxial surface of blade gla-
brous, abaxial surface of blade bearing scattered.
small brown, substellate scales 0.2-1 mm diam.
with glandular marginal cilia. Fertile frond 20—35
em long, equaling or slightly shorter than sterile
frond; stipe slender, slightly longer than sterile
stipe; blade linear-elliptic to linear-obovate, base
narrowly cuneate, decurrent, apex acute, mucron-
ulate. Spores 40-45 X 30-35 um (excluding per-
ispore), perispore cristate, crests pm high
rounded, margins entire to finely sinuate.

Distribution and habitat. Réunion; also known
from Madagascar, Comoro Islands, and Zambia. On
Réunion E. coursii is known from 400 to 2000 m
and is epiphtyic or saxicolous in open wet forests
and ericoid formations.

Elaphoglossum coursii greatly re-
sembles E. acrostichoides, but it can be distin-
guished by its darker, lustrous, and stiffer rhizome

Discussion.

scales.

Specimens examined. REUNION. Cilaos, au desst

des Thermes, Cadet 4126 (REU);

Cirque de Cilaos caldera, N of Entre-Deux & Ravine des

Dimitile, SE rim of

Citrons, Lorence et al. 7561 (MAU, PTBG);
ment, sentidr Rouhan & Grangaud 199 (P);
Benoit, cratere, Bosser 21012 (P).

Grande Ju-
aut de Saint

4. Elaphoglossum heterolepis (Fée) T. Moore.
Index Fil.: 10. 1857. Acrostichum heterolepis
Fée, Mém. Foug., 2: 56, tab. 84.

non Acrostichum heterolepis Baker,

. Fil. 521. 1874. TYPE

Flora Mixta 281 3 designated by

Rouhan & Lorence (2003: 838), PR). Figure

.

auritius. Sieber

Fronds caespitose, spaced 4—10 mm, borne in 2
ranks; rhizome short-creeping, 4—5 mm diam., pro-
fusely branched, densely paleaceous; scales 6-12
X 0.5-0.7
to black with clear or white borders, spreading. per-

mm, narrowly ovate, shiny dark brown
sistent, base cordate to auriculate, apex slender,
acute, margins entire, i
opaque (Fig. 5A). Phyllopodia 3-6 em long, choc-
olate to blackish brown, bearing at base scales as

central cells fusiform,

in rhizome; sterile fronds 22—40(—55) ст; stipe 7—
14(—16) em, 1.5-2.5 mm diam..
brown, canaliculate, winged in distal half, densely

reddish to orange-

paleaceous with reddish brown to black, narrowly

ovate, often falcate scales 3-6 X 0.5-1 mm, base

truncate to auriculate and bearing a few hair teeth,

pex long-acuminate, margins entire, scarious,

e

whitish to yellowish; blade linear-ovate to linear-
elliptic or linear-obovate, 20—40(—50) х 2.6—3.6(—
4) em, base narrowly cuneate, attenuate, apex long-
acuminate to caudate, chartaceous, costa
prominulous and rounded abaxially, prominulous
and shallowly canaliculate adaxially, bearing ba-
sally scales as in stipe, margins rounded, slightly
revolute, veins unbranched or bifurcate, apically
free, tips thickened, both surfaces of young blade
covered by a thin continuous layer of appressed,
beige to gray scales of two types, the small ones
0.5 mm diam., ovate to orbicular, peltate, scarious,
sometimes with brown centers, margins densely cil-
iate-fimbriate with hair teeth (Fig. 5C), the larger
scales often concentrated along the costa, 1.5-3 х
0.5 mm, narrowly ovate, sometimes with brown cen-
ters, base flabelliform, margins densely fimbriate-
ciliate, the cells thin-walled, translucent (Fig. 5B).
frond 34—
2) cm long: stipe 1.5 times longer than sterile

stipe; blade 14-25(228) х 1.4-2.5(-2.8) em, lin-

cuneate

adaxial blade surface glabrescent. Fertile f

ear-elliptic, base narrowly to attenuate.

apex acute to obtuse, adaxial surface blade and ab-
axial surface stipe bearing dense layer of rusty-col-
ored scales as in sterile frond, inte 5
scales very often present. Spores 43-45 x 23-30

um (excluding perispore), perispore cristate, 5—10

Annals
MESE 5 Garden

Figure 2. Habit of some Mascarene 5 species. Except for E. heterolepis, all the illustrations show
specimens with sterile and fertile fronds. — 7. heterolepis with its bi- colbre d stipe scales and both surfaces of
young blade covered by a thin continuous layer of appressed, beige to gray scales, from Mauritius, same population as
Rouhan 177. —B. Typical longer fertile aa of E. lepervanchei from Mauriti tius, same population of Aouhan et al.
17 E. macropodium from Réunion, same E as Rouhan et al. 232. —E. E. tomentosum from Mauritius,
same iS population as Rouhan et al. 180. Scale bars = 2 em.

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

шт high with finely crisped margins and spinulose
surface.

Distribution and habitat. Réunion and Mauri-
tius. Epiphytic to 10 m above ground or occasion-
ally terrestrial, often forming dense clumps, rarely
Common on both islands from 200 to
1400 m elevation in moist and wet forests.

saxicolous.

Discussion. This species resembles Elaphoglos-
sum tomentosum by the blade covered by a thin
continuous layer of appressed scales. Nevertheless.
E. heterolepis differs clearly from all other Mascar-
enes species by its apically free veins, two types of
frond scales, and slender, elongated bicolorous rhi-
zome scales with dark centers and whitish borders.
On Mauritius it
(Lorence, 1984).

Since Elaphoglossum heterolepis is similar to E.

hybridizes with Æ. tomentosum

tomentosum, Baker did not distinguish both species
in his book Synopsis Filicum (1874). Therefore, in
his treatment the name Acrostichum heterolepis Fée
appears as a synonym of the earlier published name
A. tomentosum. Consequently, А. tomentosum was
misapplied and used in place of the correct name
E. heterolepis in the following treatments: Acrosti-
chum tomentosum sensu Bojer, Hortus Maurit. 413.
part 1: 85.
1895, non Acrostichum to-

—

1837: sensu Cordem., Fl.
1891, Fl. Réunion. 96.
mentosum Bory ex Willd. Elaphoglossum heterolepis

Réunion,

is also the correct name for plants misidentified by

Tardieu as E. obductum (Каш) T. Moore and fig-
ured in her treatment in Notul. Syst. 15(4): 4:
tab. 3(6-11). 1959. Typification of the name E. het-
erolepis is discussed in greater detail by Rouhan
and Lorence (2003)

Selected specimens 5 8 Alexan-
dra Falls, Rouhan et al. 177 (MAU, NY, P); Bel Ombre.
Lorence 1402 (MO); Kanaka 8 1 ез s
А Lorenc e 1420 in MAU 1 (K,
d in 6775 к T
6. sentier е à la б aux Jones,
Кадай et al 179 (MAU. “Р, PBC): Mare Longue
Plateau. Lorence 2.11 (MO); м Lagrave, ; flank. Lorence
783 in MAL
; Pétrin Nat. Re-
rand Bassin, Loue in int 15816 ( (M. AL.
MO, REU); Piton Grand Bassin
(MAU); Piton Grand F
YU ЛЕ rd. to

ЛАП); Bassin Mor ph from ee Mares,
MAU 14609 (MAU). RÉUNION. Basse Vallée Phi-
lippe), Cadet es 192 ы, Bébour, path to Prion Bé-
bour, Lorence in MAU 15645 (MAU); Boucan Launay,
э 800 (P); Brülé de Sainte Rose, Badré 985 (P [2)):

3rúlé, Bédier 53 (P); Chemin Arnoux, Cadet 880 (P); Ci-
den Cadet 1930bis (P); Dimitile, ease in & Grangaud
02 : Mare Longue-St. Philippe Schlieben 10934

MA

I
15619 (MAU): Plaine des Fougères, 1850, Boivin s.n. (P):

Route du Grand Etang, Badré 896 (P); Salazie, 1886, Kel-
ler s.n. (P); Takamaka, € 1702 (P); Tremblet, Rouhan
& Grangaud 211 (NY, P).

8. Elaphoglossum Xheterophlebium Lorence

[Elaphoglossum heterolepis (Fée) T. Moore X
Bory ex Willd.) H. Christ].
Fern Gaz. 12: 343, fig. 2. 1984. TYPE: Maur-
itius. Pétrin Nat. Reserve, 1973, D. H. Lorence
14.2 in MAU 15821 (holotype, MAUN.

E. tomentosum

Fronds caespitose, borne in 2 ranks; rhizome
short-creeping, 5 mm diam., occ pr: branched,
densely paleaceous; scales 5—7 ).5-0.7
narrowly ovate to lanceolate, ЕВ falcate, cas-
taneous, thick, base cordate.

mm,

apex long-acute, fili-
orm, margins scarious, bearing sparse short hair
teeth or rare glandular cilia, cells opaque. Phyllo-
podia 1-2 em long, dull brown, paleaceous as in
rhizome: sterile fronds 33-45 cm: stipe 8-13

1.5-2 mm diam., stramineous, adaxially flattened.
densely о when young, scales narrowly
ovate, falcate, 2—5 1.5 mm, base peltate and
obtuse, or UH a cordate or auriculate, apex
acute, centers dark castaneous, opaque, margins
fimbriate to ciliate-dentate
with hair or glandular-tipped teeth; blade oblong-
elliptic or lanceolate, 22.5-32 x
narrowly cuneate, apex acute to slightly acuminate,

scarious pale brown,
2.6-3.4 cm. base

subcoriaceous, costa prominulous on both surfaces,
rounded abaxially, slightly canaliculate adaxially.
margins rounded, slightly revolute, veins bifurcate,
in part free with thickened tips, in part anastomos-
ing into intramarginal ares, both surfaces of blade
covered by a thin, persistent homogeneous layer of
closely appressed, matted, ovate to subcircular, pel-
0.5-1 X 0.5 mm, buff-colored, hyaline,
base and margins fimbriate with arachnoid cilia
0,1—0.3 mm long with purp or bulbous tips,

tate scales

cells thin-walled. Fertile frond 32.5-36 cm long:
stipe 16.5-19.5 em long: blade er 5 X 1-1.5

em. linear-elliptic, base and apex acute. adaxial
blade surface bearing thin layer of scales as in ster-
ile frond. Normal spores 35-38 X 25-27 um (ex-
cluding perispore), perispore cristate, 2-3 jum high
52%-85% of

with minutely spinulose margins;
spores aborted.

Distribution and habitat. Mauritius, known from
four scattered localities on the central plateau at 600
to 700 m in wet forests and Philippia Klotzsch heath
formations. In all cases, the nothospecies was grow-
ing terrestrially close to one or both parental species.
E. heterolepis and E. tomentosum.

Discussion. Specimens of Elaphoglossum Xhet-
erophlebium are remarkably uniform morphologi-

548

Annals of the
Missouri Botanical Garden

cally. Although tending to resemble E. heterolepis
somewhat more than E. E. Xhetero-
phlebium is intermediate between both parents re-

tomentosum,

garding color and shape of the scales and the veins,
which are in part free with thickened tips (resem-
bling E. heterolepis) and in part uniting into intra-
marginal ares (resembling FE. tomentosum).

Specin pin examined. MAURITIUS. Brise Fer rd., Lor-
ence 16.2 in MAU 15819 (MAU); Plaine Champagne, Lor-
ence sub PS 15099 (MAU), Lorence 996 sub MAU 16518

U), Lorence 1544 (MAU, MO); Pétrin Nat. Reserve,
Lorence 14.2 in MAU 15821 (MAU).

9. Elaphoglossum hybridum (Bory) Brack., U.S
Expl. Exped., Filic. 16: 69. 1854. Ac 1 и
hybridum Bory, Voy. Iles Afrique. 3: 95. 1804
non 5 е (Вогу) Т. Мооге,
Index Fil.: 10. . Olfersia hybrida (Bory)
C. Presl, Tent. а. 235. 1836. ТҮРЕ: Bour-
bon [Réunion]. Caverne le Gentil, Bory de St.
Vincent s.n. |НЬ. Bory 27,7] (holotype, P!). Fig-
ure 4A

з

Although the specific epithet Aybridum means
“of hybrid origin,” its application to this taxon is
The author of the basionym, Bory, does
not explain why he chose this specific epithet. Fur-
thermore, no evidence supports a hybrid origin for

not clear.

this species, as the morphology is not intermediate
between other species in the region, and the spores
are not aborted. The names Ё. hybridum var. cu-
neatum Bonap., E. hybridum var. melanopus Farw.,
and E. hybridum var. nitidum (Liebm.) H. Christ
have been applied to plants outside the Mascarene
area and are not considered herein.

9a. Elaphoglossum hybridum (Bory) Brack. var.
hybridum

Acrostichum ind Desv., Ges. Naturf. Freunde Berlin
ag. esten Entdeck. Gesammten Naturk. 5: 310.
1811, non Acrostichum ciliatum C. Presl, Reliq.
Haenk. 1: 15. 1825. TYPE: Bourbon [Réunion]. Р.
Commento s.n. (lectotype, designated by E. Schelpe
1969: 32), ЖП LOOOA!).
Elaphoglossum tricholepis (Baker) C. Chr., Index. Filic.:
17. 1905 Acrostichum oS Baker, J. Bot.
5. 1891. TYPE: Madagascar. Bekilus Mtns.,
J. T Last s.n. (holotype, K).

Fronds densely caespitose, borne in 4 ranks; rhi-
zome very short-creeping, 10-12 mm diam., un-
1-3

scarious,

branched, densely paleaceous; scales 5-10 X
mm, narrowly to oblong-ovate, brown,

base truncate to cordate, apex long-acuminate,
margins entire or with a few short teeth, base with
several short bulbous-tipped cilia, cells squarish to

linear-oblong. Phyllopodia 8-18 mm long, swollen

basally, black; sterile fronds 25—30(—55) cm; stipe
7-12(-20) cm, 1-2 mm diam., stramineous to pale
brown, slightly canaliculate, bearing a dense layer

( subulate, dark brown

©

f жыз, persistent,

scales 2—5 X 0.3-0.5 mm, base cochleariform and
closed, apex long-acuminate, filiform, margins in-
volute, entire, stipe also with simple capitate and
irregularly branched hairs; blade ovate to narrowly
ovate, elliptic, or sometimes obovate-oblong, 15-
20(40) & 3.5—4.5(-6) em, base narrowly to broad-
ly cuneate or sometimes rounded, apex acute to
acuminate, chartaceous to coriaceous, costa prom-
inulous and rounded abaxially and bearing scat-
tered subulate scales as in stipe, shallowly canalic-
ulate and glabrous adaxially, margins revolute,
bearing fringe of dark brown, spreading, persistent,
subulate scales as in stipe, veins prominulous, un-
branched or 1 to 2 times dichotomous, apically
free, tips thickened, both surfaces of blade bearing
short, numerous, simple capitate and branched
hairs, adaxially glabrescent. Fertile frond shorter
than or nearly equaling sterile frond, 16-26(-33)
cm long; stipe slender, about equaling sterile stipe;
blade 7-12 x cm, narrowly ovate to nar-
rowly elliptic, base acute to narrowly cuneate, apex
acute, adaxial surface with short capitate hairs.
Spores 36-38 X 23-25 um (excluding perispore),
perispore cristate, crests 3-7 jum high, margins sin-
uate, somewhat erose.

Distribution and habitat. Mauritius (400—900
m) and Réunion (600-2200 m); also Madagascar,
Comoro Islands, tropical and southern continental

rica, Fernando Po, Tristan d'Acunha, and Gough
island: In the Mascarenes usually found growing on
mossy rocks and boulders, rarely terrestrially, in
shade of montane wet and cloud forests.

Discussion. Elaphoglossum hybridum var. hy-
bridum can be distinguished by blades 3.5—4.5 cm
wide, absence of hydathodes, and blades with both
surfaces and margins bearing dark brown, spread-
ing, subulate scales.

Elaphoglossum hybridum var. hybridum greatly
resembles E. erinaceum (Fée) T. Moore from the
Neotropies (Moran & Smith, 2001). Phylogenetic
analyses based on molecular data are inconclusive
concerning the relationship between both species
(Rouhan et al., 2004). Although both species show
morphological characters so similar that distinction
is very difficult without knowing the geographica
origin, evidence is inconclusive if E. hybridum may
really be conspecific with E. erinaceum (in which
case, E. hybridum would have priority).

Selected specimens examined. MAURITIUS. Bassin
Blane crater, Julien in MAU 16494 (MAU); Corps de Gar-

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

549

de Mtn., anes in MAU 11498 (MAU); Mont Deux Ma-
melles, Lorence in MAU 15024 (К, MAU, P. REU); Plaine
башыл a rd., headwaters of Riviére Saint
Denis, Julien in MAU 14595 (MAU); Rivier du Poste near
Kanaka. Staub in MAU 11348 (MAU); Ruisseau Com-
Rouhan et al. 195 (P); Tamarind Falls reservoir,

] За (MAU); valley of Cascade 500
s. Lorence 1608 (MO). REUNION. Bébour, Riviere
des Marsouins, Lorence in MAU 15625A—D (MAU); sentier
de la Riviére, Rouhan & тодош 250 (Р);
tier GR RI entre “Le Bloc

Cilaos, sen-
et le gite de la 2 erne Du-
four, Rouhan 217 (NY, P, PTBG); sentier allant à la cas-
cade de Bras Rouge, Rouhan 239 (P); Dimitile, paola de
a Grande Jument, Rouhan & Grangaud 198 (P); Grand
Matarum, Lorence in MAU 15626 (MAU); Morne des Pa-
ates Durand, Lorence in MAU 15622 (MAU а
Neiges же Lorence in MAU 15635 (MAU);
Fougeres, Rouhan et al. 228 (NY, Р); Saint- 1 Gia:
se Vallée. Badré 1005 (P); Takamaka, trail to Ilet à B
Lorence & Rolland 6944 (PTBG): volcan.
Fouqué, Cadet 1556 (isolated fertile frond, Р);
Volean, Bosser 11857 (P).

anes,

Créte du

9b. Elaphoglossum hybridum var. vuleani (Le-
pervanche ex Fée) Н. Christ, Neue Denkschr.
Allg. Schweiz.
36(1): 104. 1899, Алашан all var.
vulcani Lepervanche
4l, tab. 9(3). 1844 11845], "TYPE:

[Réunion]. Plaine des Palmistes,

Ges. Gesammten Naturwiss.

"ou

Bouchon
Plaine des
afres, Jun. 1831, P. Lépervanche-Méziéres s.n.

[Hb. Bory 27.7] (holotype, P!).

Sterile fronds 8-12(-21) cm long; stipe 3-6(-13)
cm long, 0.5 mm diam., somewhat fle xuose, densely
paleaceous with small scales 2-3.5 X 0.5
large cells, short brown, capitate bis also present:
blade ovate to ovate-elliptic, 4-6(-11) х 1-2.5-
3.6) cm, surfaces scattered with abundant, short.

5 mm with

pale brown, capitate, simple or branched hairs,
margins fringed with squarrose subulate scales 1.5—
2 mm long. Fertile frond 4 X 1.3-1.5 cm, blade
with sporangia often absent from margins and ex-
treme base of

Distribution and habitat. Réunion; also Mada-
gascar and the Comoro Islands. This diminutive va-
riety is restricted to higher elevations (1300—2300
m) than variety hybridum. It is usually found grow-
ing on shady, mossy rock faces and in grottos.

Discussion. Plants of variety vulcani differ from
those of variety hybridum in their smaller habit and
fronds, in the smaller scales, and in the fertile frond
with sporangia often absent from margins and the
extreme base of the blade. Elaphoglossum hybri-
dum var. vulcani may, however, represent a depau-
perate ecotype, since collections Nene ste be-
tween variety hybridum and variety vulcani occur
on Réunion (e.g., see under var. hybridum: Bébour,

Lorence in MAU 15625A—

Riviére des Marsouins,
). MAU)

Selected specimens examined. REUNION. Cilaos, sen-
tier GR RI, entre “Le Bloc” et le gîte de la Caverne
Dufour, Rouhan 214 (NY, P); Cratere Commerson, Rouhan
& Grangaud 219 (P, PTBG); Pas de Bellecombe, Rouhan
222 (NY, Р); Pas des Sables, Sep. 1892, Cordemoy s.n.
(P): a : Piton des Neiges, near le gite, Lorence in MAU
15635 i pia sau Kerveguen, Badré 960 (P); Route
be de * ligne Domaniale, Lorence 2496
(MAU); Ni in His Grand Bénard, 16 Feb. 1847, Boivin
s.n. (P)

'elave,

10. Elaphoglossum lanatum (Bojer ex Baker)
199, fig. la-g. 1976.
Acrostichum viscosum Sw. var. lanatum Paler
ex Baker, Fl. Mauritius: 512. 1877

Maurice [Mauritius]. Bois Chéri, W. Bojer s.n.
pro parte, 4 left-hand specimens only (holo-

type, K! [Hb. Hook.]). Figure ЗВ.

Lorence, Fern Gaz. 11:

mm, borne in 2 ranks: rhi-

2-3

densely

Fronds spaced 3-5

zome short-creeping, mm diam.. rarely

dades resinous, scales

2-2.5 X 0.3-0.5
КЕ stiff, paler brown basally, base cordate to au-

paleaceous;

E

5 mm, narrowly ovate, castaneous,
riculate, apex narrowly acuminate, filiform, margins
sinuate to shortly dentate bearing short, glandular
teeth, cells square to rectangular, arranged in lon-
gitudinal rows (Fig. 6A). Phyllopodia 3-5 mm long.
swollen, dark brown, resinous, densely paleaceous
as in rhizome; sterile fronds (6—)12—30(—42) cm:
stipe (224—-12(-15) em, 1-1.5 mm diam.,

neous, slightly canaliculate, often narrowly winged

strami-

distally, when young bearing densely matted, pale

n brown, scarious, lanceolate to deltoid scales

X 0.2-0.4 mm, base truncate to auriculate, the
me prolonged into long, often bulbous-tipped cil-
ia, apex long-acuminate, filiform, margins with

опе, spreading, usually paired cilia, cells rectan-
gular; blade pendulous, narrowly to linear-elliptic,
(4—)8-20(-30) × 1-2(-2.5) cm, base narrowly cu-
neate to long-attenuate, decurrent, apex acute to
obtuse or rounded, subcoriaceous to coriaceous,
costa rounded on both surfaces, stramineous, mar-
gins rounded, revolute, pale, veins indistinct, bi-
furcate, in part apically free, in part uniting into an
intramarginal commissure, both surfaces of blade
at first densely covered with arachnoid-tomentose
layer of matted, pale reddish brown to buff-colored,
deltate to rounded, hyaline scales 0.5-1 mm diam.
(cilia included), base auriculate to sagittate, each
lobe fringed with 3 to 5 long, spreading or crinkled,
arachnoid hair teeth, apex filiform, margins bearing
| to 2 pairs of long hair teeth and shorter teeth,

cells toward base squarish to amoeboid, those to-

Annals of the

Missouri Botanical Garden

Fa :

2
36

<

Figure 3. Habit of some Mascarene Elaphoglossum speci
same population as Rouhan 218. —B. Fronds of F.
tomentose
with fertile

с. splendens on mossy boulders from Réunion,
lanatum: some
fronds,
Réunion,

of them are densely covered with arachnoid-
ayer of matted, pale scales, becoming p from Mauritius, Rouhan et al. 192. —C
from Réunion, 5 Ea Grangaud 224. —D.

|. E. rufidulum
stipitatum on rocks with fertile fronds, from
same population as Aouhan 212. Scale bars = 2 cm.

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

ward apex rectangular (Fig. 6B), adaxial blade sur-
face glabrescent. Fertile frond (3-)8-14(-20) cm.
slightly shorter than sterile frond; stipe slender,
(2-)4-8(-11) em; blade 5-7(-8.5) X 1-1.2(-1.4
cm, chartaceous, shape and scales of adaxial sur-
face as in sterile frond. Spores 35-38 X 23-28 рт
(excluding perispore), perispore cristate, crests 4—
8 um high, margins finely erose-dentate.

Distribution and habitat. Endemic to Mauri-
tius, where it is restricted to nearly vertical river
banks and cliff faces, often in sheltered overhangs
growing on soil or decomposing lava rock at 300 to
800 m.

There is a Bojer s.n. sheet housed in К (not the
sheet of the type) comprising three different spec-
imens: the right-hand specimen is E. lancifolium
and occurs in Réunion and Mauritius, but the two
remaining specimens are E. lanatum, which is en-
demic to Mauritius. Consequently, the locality of
Bourbon [Réunion] mentioned on the label of this
sheet is probably erroneous or collections were
mixed between both islands, because no other col-
lections of E. lanatum are known from Réunion.

Discussion. The holotype of Acrostichum viscos-
um var. lanatum, W. Bojer s.n pro parte, includes
4 left-hand specimens only; the 2 remaining right-
hand specimens are fertile fronds of Е. lancifolium
(Desv.) C. V. Morton (Lorence, 1976a: 199). Ela-
phoglossum viscosum (Sw.) J. Sm. is a
stricted to the Neotropics.

species re-

Extremely variable are frond size and shape, the
degree to which the veins are free or unite intra-
marginally, and the percentage of aborted spores.
This variability suggests a possible hybrid origin
(Lorence, 1976a, 1984

Although extremely variable, E. lanatum can be
distinguished from all others in the Mascarenes by
the blades with veins in part apically free, in part
uniting into an intramarginal commissure, and by
blades bearing an arachnoid-tomentose layer of
matted, pale reddish brown, deltate to rounded, hy-
aline scales. Furthermore, it is unique in being the
only Mauritian Elaphoglossum that is rupicolous
and grows exclusively on vertical river banks and
cliff faces composed of decaying lava.

In the Mascarenes, Elaphoglossum lanatum hy-
bridizes with E. hybridum forming E. Xsetaceum,
and with E. tomentosum resulting in E. Xadulter-
inum (Lorence, 1984).

elected specimens examined. MAURITIUS. Bel Om-
bre, Lorence 1406 (MAU, MO); Black River Gorge, N edge
behind Plaine Liévre, p Me in MAU 15533 (MAU, MO,
EU): Cascade 500 Pieds near Plaine Champagne. Lor-
ence 1173 (ККА, MAU, MO); Florin, le long de la V

x Riz, Rouhan et al. 192 (MAU, NY, р, РТВС);

м
A E

lare
Le

A Mtn., near summit, Lorence 21.1 in MAU 16280
foe 7 d Plateau, Lorence in MAU 15243 (К.
„ REU) Reserve, Lorence 17.2 in
MAU. 72 aU. MO): de la rivière
Rouhan et al. 194 (MAU, NY, P [2], PTBG): Tamarind
s Reservoir, Lorence in MAU 15823 (MAU). RE-
UNION? [Doubtful]. Without precise locality, Bojer s.n.
(pro parte, left-hand and center collections, K).

Cogliano,

11. Elaphoglossum lancifolium (Desv.) C. V.
Morton, Contr. U.S. Natl. Herb. 38: 32. 1967.
Acrostichum lancifolium Desv., Naturf.
Freunde Berlin Mag. Neuesten Entdeck. Ges-
ammten Naturk. 5: 310. 1811. TYPE: Mas-
careignes. 1801, A. Du Petit-Thouars s.n. (ho-
lotype, P-JU 1004!). Figure 4B

Ges.

Ac rostichum salicifolium Willd. ex Kaulf., Enum. Filic.
1824. Elaphoglossum н о
icifolium (Willd. ех Kaulf.) C. C rans. Linn. Soc.
London, Bot. 7: 421. 1912. з salicifol-

is Alston, in Exell, Cat. V
Pl. San Tomé 92. 19 E la i d йыт

(Sw.) Urb. subsp. d (Willd.

Schelpe, Contr. Bolus Herb. 1: s

Bourbon [Réunion] R. De

right-hand

asc.

au
1969. TY PE:
esfontaines s.n. pro parte,
specimen only (holotype, B-W 19509!).

Fronds spaced 4—5 mm distant, borne in 2 ranks:
rhizome short-creeping, 3-4 mm diam., sparsely
A densely paleaceous, resinous; scales 3—

50.8 mm, dark
A pens, shiny, base truncate to cordate or
auriculate, apex long-acuminate, filiform, margins
enlire except w

narrowly to linear-ovate,

ith a few short cilia and glands ba-
sally, cells fusiform. Phyllopodia 5-7 mm long.
slightly swollen, blackish brown; sterile fronds 25—
4044) em; stipe 4—10(-23) em, | mm diam., stra-
mineous to reddish brown, slightly canaliculate.
with scattered, substellate to elongate scales to 0.5—
3.5 X 0.5-1 mm, margins with long hair teeth, stipe
also with brown resinous punctations; blade linear-
elliptic to linear, 20-30(235) X 1—

narrowly cuneate to cuneate, sometimes decurrent,

(2.5) em, base

apex acute to long-acuminate, chartaceous to sub-
coriaceous, costa prominulous and rounded abaxi-
ally. canaliculate adaxially, margins revolute, veins
prominulous, unbranched or bifurcate, apically
free, tips thickened, dark, both surfaces of blade
when young with sparse, scattered stellate scales
0.5-1 mm diam., pale brown, margins with usually
6 to 8 long hair teeth, scales denser along costa.
blade surfaces also with scattered light brown, res-
inous punctations. Fertile fr p equaling or slightly
longer than sterile frond, 20-35(40) cm;
slender, equaling to twice as e as sterile stipe;
blade 14-26 X 0.7-1 em, linear or linear-elliptic,
base cuneate, apex acute, adaxial surface with scat-
tered stellate scales. Spores 35-38 X 25-28 um

stipe

Annals of the
Missouri Botanical Garden

IA ›
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Fo
» En n
С YA ч
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Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

кешш perispore), perispore cristate, crests 3—
5 pm high, margins entire to sinuate.

Distribution and habitat. Mauritius (300—800
m) and Réunion (100-1300 m); also Madagascar,
Comoro Islands, Seychelles, San Tomé, and tropical
Africa. Occurring in moist to wet forests in light to
dense shade, epiphytic to 10 m above ground or
growing on fallen trunks and mossy boulders.

Discussion. Elaphoglossum lancifolium resem-
bles E. richardii by the blade shape but differs by
its densely caespitose fronds and blade with free
veins. Elaphoglossum lancifolium can be distin-
guished from all others by scales that are stellate
with usually 6 to 8 long, straight hair teeth.

The type of Acrostichum salicifolium, R. Desfon-
taines s.n., includes the right-hand specimen only.
The remaining left-hand fertile specimen, an iso-
lated fertile frond without rhizome, is of uncertain
identity.

Acrostichum lancifolium Desv. is the oldest avail-
able name for the species (Morton, 1967: 32—33).
Morton (1973: 215-216) further stated that A.
ductum Kaulf. ex Spreng. (Syst. Veg. (ed. 16): 34.

ob-

1827) is a superfluous name based on the same
“It is likely that Kaul-
fuss intended his A. obduc tum to be based on Maur-

type as A. lancifolium Desv.:

2

itius, Sieber, Syn. Fil. no. 25 [referring now to E.
tomentosum (Bory ex Willd.) H. Christ]. and it has
been perhaps generally so considered, although
never definitely lectotypified. But when Sprengel
published the name he did not mention Sieber or
indeed cite any specimens, merely citing [errone-
ously] Acrostichum lancifolium Desv. as a synonym.
Since the name A. lancifolium was a legitimate and
available name, there was no need to propose a
different name, A. obdu pc re
[modern equivalent in the
2000: Art. 52] of the Code E name A. obductum
must be considered superfluous, and by Art. 7 [7.5]
it must be typified on the basis of the name that
ought to have been adopted, thus on the type of A.
lancifolium." Consequently, the name Acrostcihum
obductum or its combination Elaphoglossum obduc-
tum (Kaulf. ex Spreng.) T. Moore (Index Fil.: 124.
1857), has been widely misapplied. Elaphoglossum
tomentosum is indeed the correct name for the plant
identified by almost all authors as Acrostichum
Elaphoglossum) obductum sensu Kaulfuss (even if

never published by Kaulfuss himself), which is dif-
ferent from Acrostichum (Elaphoglossum) obductum
sensu Kaulfuss ex Spreng., because according to
the Code the latter name is illegitimate and must
now refer to Elaphoglossum lancifolium. The fol-
lowing misapplied name found in the early Mas-
carene literature should refer to E. lancifolium: Ac-
rostichum Bojer, Hortus Maurit.
412. 1837, Mauritius 512. 1877,
sensu Cordem., Fl. Réunion, part 1: 83. 1891, FI.
Réunion 94. 1895, non Acrostichum viscosum Sw.,
Syn. 10: 193. 1806. Elaphoglossum viscosum (Sw.)
J. Sm. is a Neotropical species.

viscosum sensu

sensu Baker, Fl.

Selected specimens examined. MAURITIUS. Bassin
Blane, Lorence 506 (MO); Bel Ombre, N of Bon Courage
forest station, Lorence & Florens 7017 (MAU, PTBG); Bois
Sec near Grand ep (date?). Lorence s.n. (MO); C
pipe, Kanaka, Bijoux 69 in MAU 2570 (MAU); Les Mares,
Rochecouste & Orian s.n. (M Er Mac е Réserve de Bri-
se Fer, Rouhan et al. 187 (MAU, P); Macabé, we men-
ant à la Mare aux D эке el 181 (MAU,
Mare enn ke os au, Mare Longue-Macabé rd., uc

7.3 in MAU 15813 (K, MAU, M, MO, P REU): Mt. La-
E fank, Lorence 792 in MAU 5 ad ); Perrier

grave,

Reserve, Rouhan et al. 193 (MAU, Р); Pétrin Nat.
dn түе, [pie 8.5 x Piton du iud Lorence 3
(MO); Piton du Milieu, Lorence 10.3 (К. MAU. MO, P):

Piton Grand Bassin, Julien in MAU 14594 (MAL); Plaine
Paul, Vaughan in MAU 12544 (MAU); Riviére Cogliano
near Mare aux Vacoas, Lorence 1374 (MO); Rivière des
Galets, below Cascade 500 Pieds, Lorence 1479 (KRA, M.
E REUNION. Bois Blanc, Guého in MAU 15362
(MAU); Cascade de Bras Rouge, 8 0 236 ee Р,
PTBG): Cilaos, au dessus des mes, Cadet 4127
(REU); red Rouhan e Pena 201 (NY, P); ah
du Grand Brúlé, Cadet 319 bis (P); Grande Jument. Rou-
han & Grangaud 197 (Р); Hauts des Trembles. Bosser
20624 (P); Morne des Patates Durand, Lorence in MAI
15628 (MAU); St. Philippe, forét de Mare Longue, Guého
in MAU 15303 (MAU); St. Philippe, Mare Longue, Schlie-
ben 10928 in MAU 12416 (MAU); Tremblet, Rouhan &
Grangaud 210 (NY, P. PTBG); Vallée de Langevin a Grand
Galet, Cadet 3718 (REU)

—

12. Elaphoglossum lepervanchei (Bory ex Fée)
T. Moore, Index Fil.: кз 1857.
lepervanchei Bory ex Mém. Foug., 2:
tab. 9(1). 1844 с TYPE: Réunion. s. n.,
Hb. Bory 27,14] pro parte, right-hand speci-
men only (lectotype. designated by Lorence

(1976: 200), P!). Figure 2B.

Acrostichum

Lud Iv didynamum (Fée) T. Moore, Index Fil.:
. Acrostichum didynamum Fée, Mém. Foug., A

igure 4. Habit of some Mascarene Elaphoglossum species
with a el E from Réunion, same population as Rouhan et n 228. —
et al. 187. C, D. E. spatulatum on mossy boulders, from Réunion, Rouhan p — 246. —C.
Sterile fronds. Scale bars = 2

fertile hands conduplicate before maturity. —D. $

E. hybridum

. ЕЁ. lancifolium, from Mauritius, Rouhan

.A. SAC at the base of a trunk,

Shows the longer

554

Annals of the
Missouri Botanical Garden

37, tab. 1602). 1844 [1845]. TYPE: Réunion. P. Lé-
p anche-Mézieres s.n. |Hb. Bory 27, 13] (holotype,

Index i
Ann. Bot. bes
C. Curtis 121 (

Elaphoglossum curtisii (Baker) C. Chr.,
ostichum curtisii n
nn TY р Ё

Madagascar. 1881,
En

а 10-
lot yhoto of ее

Elaphaglossun borbonicum (Baker) C. Chr. a Fil.:
30: ‚ Ac rostichum кили ит Baker, Ann.

: Bourbon [Réunion]. J. B. Bal-

—
^
=>

S or 1891. TYP

Jour 27 (holotype. K! !
Fronds spaced (2—)8—12(—25) mm, 2-ranked: rhi-
zome moderately long-creeping, 3—5 mm diam., oc-
casionally branched, densely paleaceous near apex:
scales 4-10 X 0.5-1 mm, narrowly ovate, elliptic
or linear, thin, pale yellowish to reddish brown,
base truncate to auriculate, apex filiform with bul-
bous tip, margins involute, bearing especially to-
ward base long. flexible gland-tipped cilia, the cells
thin-walled, rectangular to fusiform, alternating
with bands of shorter, squarish cells (Fig. 5D).
Phyllopodia 15-25 mm long, slightly swollen, ar-
ticulated, dark brown to black, paleaceous; sterile
fronds 7-35(-60) cm: stipe 2-15(-30) em X 1-2
mm, stramineous to rusty brown, slightly canalic-
ulate, narrowly winged in distal 0.5-0.7, sparsely
paleaceous, the scales loose, pale brown 1—2 mm,
margins ciliate; blade narrowly ovate-elliptic to lin-
ear-elliptic or narrowly obovate, 5-20(-26) X 1.5-
4.5(-9) em,

truncate, usually attenuate and decurrent, apex ob-

base narrowly to broadly cuneate or

tuse to acuminate, subcoriaceous to coriaceous,
costa prominulous, rounded abaxially, flattened to
canaliculate adaxially, margins thin, revolute, veins
distinct, prominulous, bifurcate 1 to 2 times, api-
cally free, tips thickened, adaxial surface of blade
glabrate, abaxial surface of blade with scattered,
appressed dark brown scales 0.2-0.5 mm diam.,
irregularly stellate with bulbous-tipped cilia (Fig.
5E), scales larger and denser along costa. Fertile
frond 12—35(—45) em long; stipe 1.5 to З times lon-
ger than in sterile frond; blade narrowly elliptic to
linear-elliptic, 6-20(-36) X 1.2-2.6(—4) cm, flexi-
ble, apex acute to obtuse, base cuneate to attenu-
ate, slightly decurrent, adaxially.
Spores 35-38 X 23-26 jum (excluding perispore),
the perispore cristate, crisped, 4—10 jum wide with

veins visible
erose-dentate margins.

Ré-

union; also Madagascar, Comoro Islands, and the

Distribution and habitat. Mauritius and

Seychelles. This species occurs in humid localities

from low to middle elevations, 200 to 900 m on

Mauritius and 160 to 1300 m on Réunion. One of

the most common Mascarene Elaphoglossum spe-
cies, it abounds in ericoid shrubland and low, open

Sideroxylon L. forests where it occurs terrestrially

or at bases of trees and shrubs. It is rarely found
in tall, shady wet forests.

Discussion. Elaphoglossum lepervanchei is ex-
tremely variable in size and shape of fronds, even
on a single plant. This has resulted in a prolifera-
tion of synonyms and misapplied names in the lit-

erature. This species resembles E. macropodium by
frond shape and reddish brown rhizome scales, but
can be distinguished by having free veins, thinner
rhizomes, and smaller rhizome scales with crisped,
involute, glandular-ciliate margins.

On Mauritius, E. Xrevaughanii is a natural hy-
brid between E. lepervanchei and E. sieberi (Lor-
1984).

The specific epithet was originally published as

ence,
“lepervanchii.” Since the species was dedicated to
Mr. Lépervanche, the publication is valid according
to the Code (Art. 32.6; € 2000), but
the Latin termination contrary 60C.1 is
treated as an orthographic error to be corrected

;reuler et al.,
Rec.

(Art. 60.11). Therefore, the correct spelling of the
name is “lepervanchet.”

In the literature concerning the Madagascan and
Mascarenes area, the following misapplied names
should actually refer to E. lepervanchet:

Acrostichum bars sensu Bojer, Hortus Maurit. 412.

1837; sensu Baker, Fl. Mauritius 12 55 1877; sensu

. Fl, Réunion, part 1: 81. 1891, FI. lanon

pos PEE non Acrostichum Bur cl Sw., Syn. Fil.
. 192, tab.1(1). 1806.

Ac 1 ad ovalifolium Bojer, Hortus Maurit. 412. 1837,
nom. nud.
Acrostichum latifolium sensu Baker,
H 77, non Acrostichum latifolium Sw.,
: 128. 1788.
apium sap sensu C. Chr., Trans. Linn.
ndon, Bot. 7: 420. 1912, non , pa
ti folium (Sv “l Sm., J. Bot.
eec i ge е sensu С 9 5 "i inn. Soc.
ndon, Bot. 7: 420. 1912; sensu Tardieu in Hum-
jit Fl. M Маа е 5(2): 35. 1960, 5
sum conforme (Sv.) J. Sm., J. Bot. 427): 148. 1841.

Fl. Mauritius 511.
Prodr. Pl. Ind.

Selected specimens examine i Succus S. Alexan-
dra Falls, Rouhan et al. 175 NY, P); Bassin Blanc,
Lorence 628 in MAU 16319 E Bassin Blanc to Les
Mares path, Lorence in MAU 14610 (MAU); Bel Ombre,
Lorence 327 (MO); Black River 5 2m Plaine Cham-
pagne, Lorence in MAU 14880 (K, MAU, P): С 5 rd.
from Plaine m e, Lorence in wi 14640 (M Pea
De diei Julien in MAU 13318 (MAU); !
. Lorence in MAU E 588 (MAU n Mare
ar: i to Macabé, 779118 in MAU 15:
^U), Rouhan et al. 188 PP ees E trin
. Reserve, rd. to Grand Bassin, 1 12.1 in MAU
s (K, MAU, P, REU), Lorence 18.3 in MAU "15812
(К, MAU, MO, P, REU); Pétrin to Macabé rd., Vaughan
in MAU "d (MAU, Р); Piton Brise Fer, Lorence 3.1 in
ien (К, M, MAL, MO, P); Piton du Fouge, Lorence 1626
MQ); Piton e: Bassin. Lorence in MAU 14589 (MAU):
Plaine Champagne to e rd., Lorence 14.1 in MAU

555

Mascarene Elaphoglossum

Lorence & Rouhan

Volume 91, Number 4

2004

EU

Réunion,

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Figure 5. Scales of some Mascarene Elaphoglossum s

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Annals of the
Missouri Botanical Garden

15811 (K, KRA, MAU, MO, P, REU); P Champagne,

S of Black River Gorges, Lorence in MAU 15010 (К, MAU,
Р): Plaine оо М of Plaine Paul, gods 2.3 in
MAU 1583 m NION. Brûlé, Bédier 52
pro parte, right- b spec imen P); n aos, au dessus des
The ermes, Сайа 4130 (REU); ү du Bébour, Lorence in
MAU 15 MAU, MO): sentier de la rivière, Rouhan &
Grangaud т (NY, Р, PTBG); Petite Plaine des Palmistes,

age igi (REU); Plaine des Fougeres, ү et al.

7 Tremblet, Rouhan & Grangaud 208 (NX. P.
= BG 3 Vallee de Langevin, Cadet 3766 1 015

—
=
m

2
~

13. о a (Fée)
oore, Index Fil.: ‚ Acrostichum ma-
cropodium Fée, Mém. 1 2.: 30, tab. 6(2).
1844 [1845]. TYPE: Bourbon [Réunion].
1844, s.n., [Hb. Bory 30, 12] (holotype, P).
Figure 2D.
Acrostichum аи Sw. var. carmichaelii Baker, Fl.
auritius: 511. 1877. TYPE: Mauritius. D. Carmi-
eds s.n. 1 K! [Hb. Hook.]).

Fronds densely caespitose, borne in 2 ranks; rhi-

zome short-creeping, thick, 10-15 mm diam., un-
branched, densely paleaceous; scales narrowly
ovate, (10—)15—25 X 2—4 mm, reddish to yellowish
brown, flat, thin, truncate to cordate at base, acute
at apex, margins bearing rare bulbous-tipped cilia,
cells linear to fusiform in vertical rows, thin-walled.
Phyllopodia 1-1.5 em long, swollen, brown to dark
brown, densely paleaceous; sterile fronds 30—55(—
13) cm; stipe 8-20(-24) cm X 3—4 mm, strami-
neous, adaxially canaliculate, narrowly winged dis-
tally, bearing scattered appressed scales; blade
narrowly elliptic to ovate- or oblong-elliptic, 18—
36(—50) X 4—6.5(—8.6) cm, base narrowly to broad-
ly cuneate, decurrent, apex acute to short-acumi-
nate, coriaceous, costa prominulous, rounded
abaxially, slightly canaliculate adaxially, margins
revolute, veins distinct, prominulous on both sur-
faces, bifurcate 1 to 2 times, uniting apically into
an intramarginal commissure, adaxial surface of
blade glabrate, abaxial surface of blade with sparse,
scattered appressed brown scales 0.5 mm diam.,
stellate with bulbous-tipped cilia, scales larger and
denser on abaxial surface of costa. Fertile frond
30-55
ly longer than in sterile frond; blade narrowly el-
Прие, 5-12(-15) х 2-4 base
broadly cuneate, apex acute to rounded. Spores 33—
38 X 28-30 um (excluding perispore), the peri-
spore cristate, the crests 4-10 um high with finely

» em, equaling sterile, stipe equaling or slight-

cm, narrowly to

spinulose-denticulate margins.

Distribution and habitat. Mauritius and Ré-

union; also tropical eastern and southern Africa,
Seychelles, and Comoro Islands. Common and wide-

spread in Réunion as an epiphyte on mossy trunks

up to 10 m above ground or rarely terrestrial, in
shade of wet forests and ericoid shrublands from 100
to 1500 m.
been collected in Mauritius since 1923 and is either
extremely rare or extirpated there [vs. Réunion].

Elaphoglossum macropodium re-

Elaphoglossum macropodium has not

Discussion.
sembles E. sieberi by the frond shape and dimen-
sions, and it resembles lepervanchei by frond
shape and reddish brown rhizome scales. Elapho-
glossum macropodium differs from E. sieberi and E.
lepervanchei by its extremely thick rhizomes (10—
5 mm diam.) densely clothed with larger, flat, thin,
subentire reddish to yellowish brown scales.

The following name was misapplied by Corde-
moy and should now refer to E. macropodium: Ac-
rostichum sieberi sensu Cordem., Fl. Réunion, part
1: 81. 1891, Fl. Réunion 93. 1895, non Elapho-
glossum sieberi Hook. & Grev, Icon. Filic. tab. 237.
|

831.

Selected аран imens examined. MAU 1 Curepipe,
Sere Bijoux 73 (P); е Nov. 1923, s.n. (pro par-

„ left-hand collec 11 7 .R D Bébour, e
ence in MAU 15638 (M AU [2 | MO); Bralé, 5 4 (P
[2]; Saint- Philippe, Bosser 9559 (P, [2]); M
Plaine des Affouches, Bosser 20432 (P); Morne des Pa-
tates Durand, Lorence in ea 15620 (MAU); Plaine des
Dos d'Ane, Bosser 22485 (P); Salazie,
“Mezieres s s.n. |Hb. Bory 30,10] (P); For-
Wong 7 (P € Grand Bénard, Boivin
n& eee 207 (NY, P, PTBG);
& Grange iud 209 (NY, P); Plaine des
Fougères, odian et al. 232 (P). Aug. 1850, Boivin s.n. (Р

~

‘thicots, sentier
1835, Lépervanche
ét du Grand 1 Bralé,

"d
—

14. Elaphoglossum Xrevaughanii Lorence
[Elaphoglossum lepervanchei (Bory ex Fée) T.
Moore X E. sieberi (Hook. & Grev.) T. Moore],
Fern Gaz. 12: 342, fig. 1. 1984. TYPE: Maur-
itius. Mare Longue Plateau, 1973, D. H. Lor-
ence 14.3 (holotype, MAU 15818; isotypes,
K!, MAU!, MEXU!, MO!, P!, REU!).

Fronds caespitose, borne in 2 ranks; rhizome
short-creeping, 5-6 mm diam., occasionally
branched, densely paleaceous; scales 3-6 X 0.5-
0.8 mm, narrowly ovate to lanceolate, black, shiny,
rigid, base truncate to cordate or auriculate with
short, glandular cilia, apex long-acute, filiform,
margins entire or rarely with a few long, glandular
cilia, the cells small, rectangular, seriate, black and
opaque. Phyllopodia 15—20 mm long, slightly swol-
len, grayish to yellowish brown, paleaceous; sterile
fronds (30—)44—53 cm; stipe 14-16(-19) em & 2-
2.0 mm, stramineous, canaliculate, when young
bearing scattered dark brown to black, appressed-
ovate to lanceolate scales 0.5—4 х 0.2-0.5 mm.
base cordate to auriculate, fringed by short glan-
dular cilia, apex filiform, sinuate, margins sinuate

Volume 91, Number 4 Lorence & Rouhan 557
2004 Mascarene Elaphoglossum
with scattered glandular cilia, cells dark brown: chardu (Bory ex Fée) Hook.. Sp. Fil. 250.

blade narrowly elliptic to linear-elliptic, (19-)30—
35 X (4.3-)5.5-7 cm, base narrowly cuneate, de-
current along distal 0.25—0.3 of stipe, apex acute
K
and rounded abaxially,

acuminate, subcoriaceous, costa prominulous

canaliculate adaxially, mar-
gins revolute, veins visible, raised, bifurcate | to 2
times, in part apically free and with thickened tips.
in part uniting into intramarginal ares, both surfac-
es of blade glabrate except for scattered brown.
glandular-ciliate scales 0.5 mm diam. along abaxial
surface of costa. Fertile frond (80—)35—42 cm long:
stipe (15-)17-22 em: blade narrowly elliptic to lin-
ear-elliptic. 15-23

base narrowly cuneate, adaxial surface

1.5-2.6 cm, apex acute to
acuminate,
pallid with minute, scattered scales, veins not vis-
1%—5% very large (15-88 X 50-00
um. excluding perispore), 65%-67% aborted.
20% 30% normal (40—50 X 30-35 um. excluding

perispore), the perispore with large. ruffled crests

ible. Spores:

10-15 um high.

Distribution and habitat. Mauritius. endemic
and known only from Mare Longue Plateau (630 m)
and Pétrin Nature Reserve (660 m)

Discussion. This natural hybrid between F. le-
pervanchei and E. sieberi possesses а high percent-
age of aborted or abnormal spores and presents
morphological characters intermediate between
species. Elaphoglossum Xrevaughanit

these two

has veins partly free (as in H. lepervanchei) and

—

partly reunited into a submarginal commissure (as
in E. sieberi). and scales on the lower portion of the
stipe and phyllopodium are intermediate between
those of both parents. The hybrid is more robust
than. either parent, which both occur in the same
biotope, usually as depauperate individuals grow-
ing at the bases of stunted trees and shrubs because
it is a marginal, suboptimal habitat for these shade-
loving. wet forest epiphytes. Obviously more suc-
cessful than either parent in this particular ecolog-
ical setting of low shrub vegetation, the hybrid
behaves like a terrestrial heliophilous or hemiscio-
philous species and apparently reproduces vegeta-

—

tively by rhizome branching (Lorence. 198

Specimens eo 18 AURITIUS. Mare Longue Pla-
teau. Lorence 11.1 (M MEXU, МО), Lorence 8.6 in
MAU 15531 (K. MAU, PS Р, REU). uM e 1176 (MO),
Rouhan et al. 190 (MAU, NY. A oe ; Pétrin Nat.
Reserve, Lorence 1497 (MAU

15. Elaphoglossum richardii (Bory ex Fée) H.
Christ, Neue Denkschr. Allg. Schweiz. Ges.
Gesammten Naturwiss. 36(1): 35. 1899. Acon-

Mém. Foug.. 2:

Acrostichum ri-

iopteris richardii Bory ex Fée,

80. tab. 16(4). 1844 [1945]. .

1864. TYPE: Bourbon [Réunion]. "Dans les
foréts sur les vieux bois." J. M. C. Richard 10
Hb. Bory 30,28] (holotype, P!). Figure 1C.

Fronds spaced 1-2 em distant, borne in 2 ranks:
rhizome long-creeping, 2-3.5 mm diam.
branched, paleaceous, resinous; scales 3-0 X
0.5 mm, linear-ovate to lanceolate, sinuate, brown
to dark brown, shiny, thin, base cordate, apex long-
acute, margins bearing short cilia or reflexed teeth
toward base, cells small, oblong-fusiform (Fig. ОС).
Phyllopodia 10-15 mm long. slightly swollen. dark
brown; sterile fronds 25—40(—55) em: stipe 6-12(—
15) em, 1-2 mm diam., stramineous to brown, when
voung bearing minute, brown resinous punctations
and abundant, ovate to oblong scales to 5 X 0.4
mm with glandular ciliate-dentate margins; blade

15-34 X 1.5-2(-3) em.

rowly cuneate, often decurrent, apex acute to ob-

linear-elliptic, base nar-
tuse, subcoriaceous, costa prominulous and round-

ed abaxially, canaliculate adaxially, margins
revolute. veins distinct, bifurcate, apically uniting
into an intramarginal commissure, both surfaces of
blade minutely paleaceous when young, scales

X 0.2-0.3

mm, pale brown, scarious, margins with hair teeth.

ovate-triangular to linear-oblong. 0.5-1

with cluster of resiniferous glands at base (Fig. 0D),
adaxial surface glabrescent leaving brown resinous
punctations. Fertile frond equaling or slightly lon-
ver than sterile frond: stipe slender, Morum de or

slightly longer than sterile stipe: blade 11-24
0.8-1.4 em, linear, base narrowly cuneate, bolt

rent. apex acute, adaxial surface paleaceous and
with resinous punctations. Spores 30-33 X 23-25
um (excluding perispore), perispore cristate, crests
2.5-5 um high, margins finely sinuous-erose.

Distribution and habitat. Réunion, endemic.
Epiphytic on mossy trees and boulders up to 3 m
above ground level in shady wet forests, 300 to
1460 m.
Discussion. The specific epithet was published

as “richardi.” Since the species was dedicated to
Mr. Richard. the publication is valid according to
the Code (Art. 32.6: Greuter et al., 2000), but the
Latin termination contrary to Rec. 60C.1 is treated
as an orthographic error to be corrected (Art.
60.11). Therefore. the correct spelling of the name
is “richardii.”

This species resembles Elaphoglossum lancifol-
ium by the blade shape, but differs by more widely
spaced fronds, blades with non-stellate scales, and
veins uniting apically to form a submarginal com-
In addition to the latter character, E. ri-
linear-elliptic

missure.

chardii can be distinguished by

558

Annals of the
Missouri Botanical Garden

scale.

Figure 6. Scales of some |
15014. —A. Rhi ale. —B
—D. Lamina se: „ЕКЕ

G, H. V. stipitatum, from

а
amina scale. . E. richardii, from

on, Bory 42 |Hb. Bory

G. Rhizome scal«

==> —
с > РУ
— — —— —

Т; ==
Бе == —
ARE

éunion, Lorence 15
б 27,28]. —E. Rhizome scale. —F. Lamina
. —H. Lamina scale. Scale bar = 1 mı

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

blades (1.5-2 cm wide), paleaceous when young

and bearing resinous punctations. The following
name misapplied by Tardieu should refer to E. ri-
chardit: * stipttatum sensu Tardieu,
Notul. Syst. 1500: pl. 2, figs. 1-3. 1959,
Elaphoglossum ne (Bory ex Fée) T.
Index Fil.: 15.

non
Moore.

RÉUNION.
lée, Ravine Pérote, Rouhan 234 (P); Bébour forest. Lor-
ence in е 14 15644 (MAU, MO): Bois des Hauts de S

Paul. (P [2]: Bouc an га 1852, Bernier s.n.
(P): rale. Bédier 56 (P). ; Chemin Arnoux, Cadet
679 (P); Hauts de l'Ouest, se 1 de l'ilet Alcide, Rouhan
et al. 244 (Р); Hauts de St. Rose (Forêt Mourouvin), Cadet

Selected specimens examined. Basse Val-

Saint-

3884 (P. REU): Le Dimitile, Rouhan «€ Grangaud 205
(NY. P. PTBC): Mare Longue forest, Lorence in MAU

15630 (MAU): Patates Durand, Lorence in
: Plaine des Fougères, Rouhan
Plaine des Palmistes, June

et al. 231 (NY, P. PT т
851. Boivin s.n. (Р).

16. a a rufidulum E illd. ex Kuhn)

Chr., Index Ее: Acrostichum
1 Willd. ex Kuhn, Filic. Afr 47. 1868.
Elaphoglossum deckenii (Kuhn) C. Chr. var. ruf-

idulum (Willd. ex Kuhn) Tardieu, Notul. Syst.
15(4): 430. pl. figs. 6-10. 1959. Elapho-
glossum hirtum (Sw.) C. Chr. var. ү
(Willd. ex Kuhn) €. Chr., Dansk. Bot. Ark.
170. 1932. TYPE: Madagascar. J-B. ee
. (holotype, B-W 19511; B-W
MO). Figure 3C.

microfiche

Fronds densely caespitose, borne in 2 to 3 ranks:

rhizome very short-creeping, 3 mm diam., un-
branched, densely paleaceous; scales 2-3 X 1 mm,
narrowly ovate, dark brown, shiny, paler basally,
base cordate to auriculate, apex acute, margins
subentire or bearing black hair teeth 0.1—0.3 mm
long, cells rectangular to fusiform with thick walls.
Phyllopodia 0.6-1 cm long, slightly swollen. dark
brown, densely paleaceous as in rhizome, but
scales with long marginal cilia; sterile fronds 23—
stramineous,

34 em: stipe 9-15 cm, 1 mm diam.,

canaliculate, densely paleaceous, the scales

spreading, pale brown to reddish brown, narrowly
X 0.

<

ovate, 3—4 5-1.2 mm, base cordate to auric-
ulate, apex acute, margins bearing pale brown to
black hair teeth 0.2-0.8 mm long, cells rectangular
to oblong-fusiform, often bifurcate apically; blade
narrowly elliptic, 13-19 X 2-2.5 ст, base narrowly
cuneate, apex short- to long-acuminate, charta-
ceous, costa prominulous and rounded on both sur-
faces, margins rounded, weakly revolute, margins
and costa bearing many, reddish brown, spreading,

0.2-0.5 mm,
apex acute, margins bearing 2 to 8 pairs of stiff,

ovate scales 1—3 base auriculate,

long hair teeth, veins prominulous, simple or bi-
furcate, apically free, both surfaces of blade cov-
ered with numerous reddish brown spreading or im-
bricated scales similar to those on margins. but
smaller. Fertile frond about as long as sterile frond:
stipe longer than sterile stipe. ca. 18 em: blade ca.
10 * 1.3 em, narrowly elliptic, base narrowly cu-

neate, apex obtuse, rounded, scales of adaxial
blade surface and both surfaces of costa as in ster-
ile frond. Spores 37-38 * 28-30 um (excluding
perispore), cristate,

perispore crests 2.5—5 um

high, margins finely sinuate-dentate.

Distribution and habitat. Réunion and Mada-

gascar. This species is rare on Réunion, where it
occurs on lava in the shade of fissures and grottos
in ericoid vegetation from 2200 to 2340 m.
Discussion.
bles K.

rhizome and frond scales with stiff hair teeth.

Elaphoglossum rufidulum resem-
splendens in general appearance and by its
but
E. rufidulum occurs at higher elevations, and its
sterile fronds are less densely paleaceous, with the
imbricated scales not completely obscuring the
frond surface. Furthermore, E. rufidulum lacks
black scales on the abaxial surface of the costa.
which are present in E. splendens. Specimens from
the Comoro Islands closely resemble and may be
conspecific with E. rufidulum, but these collections
have been referred to E. tanganjicense Krajina ex
1968: 238).

does not occur in the Mascarenes. Elaphoglossum

Pic. Serm. (see Pichi Sermolli. which
kuhnii Hieron. of tropical Africa (absent in the
Masacarenes) is also closely related. This complex,
which occurs from tropical America to Macarone-
sia, tropical Africa, the Malagasy region, and Ha-
магт, is in need of critical study.

Specimens examined. REUNION. Volcan, Massif de la
Fournaise, l'Enclos Fouqué, pres du Pas de Bellecombe.
Cadet 1535 (P, REU); Pas de Bellecombe, bord du sentier
descendant dans ГЕпс lae. Rouhan & Grangaud 224 (P).
Des Abbayes 2950 (P).

17. Elaphoglossum Xsetaceum Lorence [Hu-
Brack. X E. lan-
atum (Bojer ex Baker) Lorence]. Fern Gaz. 12:
348, fig. 5. 1984. TYPE: Mauritius.

Falls Reservoir, 1973, D. H
lotype, MAU 15823b!).

phoglossum hybridum (Bory)

r

=

"amarind
. Lorence s.n. (ho-

Plant with fronds caespitose, borne in 3 ranks:
rhizome very short-creeping, 3 mm diam., un-
branched, densely paleaceous; scales 3—4 0.5

mm, lanceolate to narrowly ovate, light castaneous.
base cordate, apex filiform, margins bearing short
cells

Phyllopodia 2—4 mm long.

teeth each terminated by a globose gland,
rectangular-fusiform.

560

Annals of the
Missouri Botanical Garden

dark brown, paleaceous; sterile fronds 8—14 сш;
stipe 3-3.5 0.5-0.7 diam.,
brown, canaliculate, bearing numerous simple cap-

cm, mm yellowish
itate hairs and abundant, brown, squarrose, subu-
late scales 1.5-2.5 X 0.2 mm, base cochleariform,
apex filiform, margins involute, bearing several long
cilia and short glandular teeth or cilia; blade nar-
rowly elliptic to narrowly ovate, (5—)9-10.5 X (1—)
1.5-2 cm, base narrowly cuneate, decurrent as low
ridges along stipe, apex acuminate, chartaceous,
costa prominulous on both surfaces, yellow brown,
both surfaces bearing spreading subulate scales as
in stipe, margins slightly revolute, rounded, ciliate
with fringe of pale brown, spreading, bristle-like
scales 2-3 0.2-0.3 base cochleariform,
apex filiform, margins involute basally and bearing

min,

several long, spreading glandular-tipped cilia and
sparse short hair teeth, veins distinct, bifurcate,
apically free, tips thickened, both surfaces of blade
villous bristle-like intermixed with
smaller flat, deltate scales, each with a single pair

with scales
of long, spreading basal cilia and scattered simple
hairs. Fertile frond and spores unknown.

Distribution and habitat. Mauritius, known
only from the type locality at 500 m in secondary
forest. A single sterile individual of this nothospe-
cies was found growing in a population of E. lan-
atum on a shady stream bank with £. hybridum var.
hybridum growing on a tree directly overhead (Lor-
1984).

Discussion.
es morphological characters almost exactly inter-
mediate between those of the putative parents, no-

ence,
Elaphoglossum Xsetaceum possess-

tably shape of the blade and scale characters.

Furthermore, E. Xsetaceum presents a rhizome
bearing three ranks of fronds, whereas E. lanatum
is a two-ranked species and E. hybridum var. hy-
bridum has four ranks (Lorence, 1984).

r

2

18. Elaphoglossum sieberi (Hook. € Grev.)
Moore, Index Fil.: 14. 1857. Acrostichum sie-
beri Hook. & Grev., Icon. Filic. tab. 237. 1831.
Olfersia sieberi (Hook. & Grev.) С. Presl, Tent.
Pterid. 235. 1836. TYPE: Mauritius. W. Bojer
s.n. (lectotype, designated by Lorence (1976:
204), K! ie Hook., pro parte, left-hand spec-

imen only]. Figure 1E.

Fronds densely caespitose, borne in 2 ranks; rhi-

zome very short-creeping, 7—10 mm diam., un-
branched, densely paleaceous; scales 8-20 X 0.5-

mm, narrowly linear-ovate, dull brown to black.

base enlarged, cordate to auriculate, distally fili-
form and often sinuate, the margins fringed basally

with short, glandular projections, medially and api-

cally entire or rarely with short, glandular projec-
tions, the cells narrowly rectangular-fusiform with
thick, dark walls (Fig. 5F). Phyllopodia 6-15 mm
long, swollen, articulated, dark brown to black, pa-
leaceous; sterile fronds 20-45(-65) ст; stipe 5-
15(-25) em X 2—4 mm, stramineous, terete, bear-
ing scattered brown to black, appressed-persistent
scales 5-10 X 0.25-0.5 mm, base stellate with
glandular cilia, apex filiform; blade narrowly ovate
—6(-9)

em, base narrowly to broadly cuneate, sometimes

to elliptic or linear-elliptic, 15-30(-42) X 4
attenuate and decurrent, apex acute to obtuse or
rounded, subcoriaceous to coriaceous, costa prom-
inulous, rounded abaxially, flattened to canaliculate
adaxially, margins revolute, veins indistinct, bifur-
cate ] to 2 times, uniting apically into an intra-
marginal commissure, adaxial surface of blade gla-
brate, abaxial surface of blade with scattered,
appressed brown scales 0.5 mm diam., stellate with
bulbous-tipped cilia (Fig. 56). Fertile frond 16-
30(—45) em long; stipe as in sterile frond; blade
narrowly elliptic linear-elliptic, 6—-20(-36) X
1.2-2.6(A) em, apex acute to obtuse, base cuneate
to attenuate, slightly decurrent, veins visible adax-
ially. Spores 35-38 X 23-26 um (excluding per-
ispore), the perispore cristate, crisped, the crests
4-10 um high with erose-dentate margins.

Distribution and habitat. Mauritius, endemic.
One of the most commonly encountered members
of the genus on Mauritius. Elaphoglossum sieberi
grows as an epiphyte to 10-12 m above ground or
casually terrestrial, in moist and wet forests and
ericoid shrublands, at 200 to 900 m.

Discussion. Elaphoglossum sieberi resembles E.
macropodium by the shape, texture, and size of the
fronds, but can be distinguished from E. macropo-
dium and all others in the Mascarenes by a thinner
rhizome (7—10 mm diam.) densely clothed with long
(8-20 mm),
black scales.

narrowly linear-ovate, dull brown to

—

Selected. specimens 5 MAURITIUS. Alexan-
dra Falls, Rouhan et al. 169 (MAU, NY, Р, PTBG); Bassin
Bl: anc, 1966, Edgerley s.n. in MAU 12464 (MAU, P); Cu-
repipe, Kanaka, 1906, Bijoux s.n. (MAU); Curepipe,
Vaughan in MAU 2566 (MAU); Deux Mamelles Mtn.,
ence in MAU 15016 (MAU); Ferney, mtn. ridge, D
1 MAU 16314 (MAU); Le Pouce Min., Aug. 1849,
Boivin s.n. (Р); Les Mares, Rouchecouste & Orian s.n.
(MAU 20: Macabé, Lorence in MAU 14584
cabé—Brise Fer rd., Lorence in MAU 14586 (MAU); Mt.
agrave, E flank, Lorence 779 in MAU 16318 (MAU), Lor-
ence 782 in MAU 16313 (MAU); Pétrin Nat. Reserve, Lor-
ence in MO M129 (MO. P); Pétrin-Les Mares rd., t

MAU 12624 e Lr Piton Combo, Lorence 890
Piton du Milieu, Lorence 10.2 in 1581.

REU); Piton Cand

(MAU,

Lorence 1074 (MO); Piton

Bassin,

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

Lorence 301 (MO); Plaine Champagne nr.
Cascade 500 Pieds, Lorence s.n. Plaine Cham-
pagne- -Chamarel rd., er rs of Rivie re Saint Denis,
MAU 14585 (MAU) Plaine M
Ombre rd., Lorence 9.1 (MO); Plaine Char
MO): Plaine Paul , near path to
Mt. Coc até, Vaughan in MAU 12593 (MAU)

Grand Fond,

19. Vra ti ge spatulatum (Bory) T. Moore,
Index Fil.: 14. 1857.
Bory, Voy. Lin Afrique. 1:
1804. Par Bourbon 195 To yu 're St.
Denis, “an X" [1801-1802]. J. В G. M.
Bory de E a s.H. Tub Bory Am (ho-
lotype, P!). Figure 4C, D.

Acrostichum spatulatum
303, tab 20, fig.

Fronds caespitose, borne in 3(to 4) ranks: rhi-
zome very short-creeping, 1.5-2 mm diam., short
and unbranched, densely paleaceous; scales 3-4. х
0.3-0.4 mm, narrowly ovate, membranaceous, red-
dish brown, base cordate to auriculate, apex nar-
rowly acuminate, filiform, margins entire, cells fu-
siform. Phyllopodia absent; sterile fronds 3—7(—9)
em: stipe 2—4(—6) cm, 0.5 mm diam.,
slightly

stramineous,
canaliculate, densely paleaceous with
spreading, narrow, reddish brown, subulate scales
2-3 X 0.3-0.4 mm,
lute, apex long-acuminate, margins with scattered

base cordate, the lobes invo-

short teeth basally, distally entire; blade narrowly
obovate-spatulate to narrowly elliptic, 1.5—4(—5.5)
X 0.5-0.8(—1.2) em, base narrowly cuneate and de-
current, apex obtuse or rarely acute, thickly char-
taceous, costa prominulous and rounded on both
surfaces, margins thin, cartilaginous, revolute,
veins bifurcate, apically free, tips thickened and
dark, both surfaces of blade and margins with scat-
tered slender, subulate scales like those on stipe
but smaller, mixed with simple capitate trichomes.
Fertile frond slightly longer than sterile frond. 5
9(-10) em long: stipe slender, often longer than
sterile stipe: blade 1-2.3 X 0.7-1 em, ovate, ellip-
tic, or obovate, conduplicate before maturity, base
cuneate, shortly decurrent, apex obtuse, often
emarginate, adaxial surface paleaceous as in fertile
frond, margins thin, cartilaginous. Spores 30-35 X
20-25 pm (excluding perispore), surface cristate,
crests 3-5 um high with entire, sinuate margins.
Distribution and habitat. Réunion, Mauritius:
also known from Madagascar, tropical Africa, extra-
tropical southern Africa, and Sri Lanka (Sledge,
1967).

union where it grows exclusively on mossy boulders

This diminutive species is common on Ré-

and rocks in the beds of rivers and streams from
900 to 1400 m. On Mauritius E.

known only from two collections made over a cen-

spatulatum is

tury ago; it may be extirpated.

Ipagne near

Discussion. Elaphoglossum spatulatum can be
easily distinguished from all other Elaphoglossum
in the Mascarenes by the small fronds 3—7(—9) em
long bearing subulate scales and the fertile fronds
conduplicate before maturity. Furthermore, H. spa-
tulatum is unique in growing exclusively on boul-
ders in the beds of rivers.

Elaphoglossum spatulatum greatly resembles .
piloselloides (С. Presl) T. Moore, a tropical Ameri-
can species (Moran & Smith, 2001), but E. spatu-
latum. differs by having the scales of the fertile
fronds orange-tan rather than black (Mickel, 2002).
The close relationship. between both species is
strongly supported by phylogenetic analyses based
on molecular data, since E. spatulatum and E. pi-
loselloides appear more related to each other than
to any other species in the genus (Rouhan et al.,
2004). Thus, E. spatulatum may possibly be con-
specific with E. piloselloides (in which case H. spa-

tulatum would have priority).

Selected specimens examined. MAURITIUS. Woods of
and Port and Savanne, [probably Bijoux]. s.d., s.n. ex
Hb. dini oid mousses s.n. (MAU). REUNION. Basse Vallée,

P +, Rouhan 235 (NY, P, PTBG): Bébour, Rou-

Pia & 5 246 (NY, Р, PTBG); Bralé, 1891, Bedier
(P); Hautes de Ste. Marie, Coode & сайи 5007

+4 AU); Montée de la Р laine a Affouch

~

Ravine Pér

—
—

bos 82 (p.
Takamaka, Guého in п MAU 15363 (M. Al чу

©

20. Elaphoglossum splendens (Bory ex Willd.)
Brack., U.S. Expl. Exped., Filic. 16: 68 1854.
Acrostichum splendens Bory ex Willd., Sp. РІ.
ed. 4, 1810. TYPE: Bourbon [Ré-
union]. An X [1801-1802], J. B. G. G. M. Bory
de St. Vincent s.n. |Hb. Bory 27,25] (holotype,
B-W 19515. B-W microfiche MO!; isotype, P!).
Figure 3A.

<

—

Fronds densely caespitose, borne in 4 ranks; rhi-
zome short-creeping, 3—4 mm diam., unbranched,
0.6-1

castaneous or dark brown,

densely paleaceous; scales 2.5-3.5 mm,

narrowly ovale, shiny,
stiff,
short hair teeth (Fig. 6E). Phyllopodia 1—1.5 ст

base cordate, apex acute, margins bearing

long. slightly swollen, dull brown, densely palea-
ceous as in rhizome; sterile fronds 25—40(—53) cm;
stipe 4—16(—30) cm, 1.5-2 mm diam., pale orange-
brown, canaliculate, densely paleaceous, the scales
spreading, dark reddish brown, ovate to linear-ob-
long, 3—5 X 0

apex acute, often black, margins bearing many dark

.5—1.5 mm, base truncate to cordate,

brown to black stiff hair teeth, cells shortly fusiform
to irregularly oblong, with thick walls; blade linear-
ovate to linear-elliptic, often falcate, 16-24(-33) X

562

Annals of the
Missouri Botanical Garden

1.52.5 3.6) cm, base narrowly cuneate to atten-
uate, apex acute, acuminate or sometimes c 'audate,
chartaceous to subcoriaceous, costa prominulous on
both surfaces, adaxially flattened to slightly cana-
liculate, abaxially rounded, margins rounded,
sometimes weakly revolute, fringed with spreading
scales, veins bifurcate, apically free, both surfaces
of blade covered with a dense, persistent layer of
imbricated reddish brown scales aging grayish
adaxially, those on abaxial surface of costa usually
dark brown to blackish, scales ovate to narrowly
ovate, (0.3—)1.5-2.5 X 0.2-0.5 mm, base cordate,
apex acute, margins fringed with long, erect-
spreading hair teeth (Fig. 6F). Fertile frond as long
as sterile frond: stipe 1 to 1.5 times as long as

blade 14-18(234) X 1.2-1.4(-1.9)

cm, linear to linear-elliptic, base cuneate, truncate

sterile stipe:

or cordate, apex acute to obtuse, scales of adaxial
surface and abaxial surface of costa as in sterile
frond. Spores 38-42 X 25-28 um (excluding per-
ispore), perispore weakly cristate, crests 2.5—4 jum
high, margins entire to sinuate.

Distribution and habitat. Réunion and Mauri-
tius. Elaphoglossum splendens is common on Ré-
union, where it occurs as an epiphyte in the shade
2350 m.

or occasionally on mossy boulders in ericoid veg-

of wet forests and cloud forests at 1000 to

etation. It is extremely rare or perhaps extirpated
on Mauritius, where it is known only from two col-
lections made in the early 1900s.

Discussion. Elaphoglossum splendens resembles
E. rufidulum in general appearance and by its rhi-
i but H.

splendens occurs at lower elevations, and its sterile

zome and frond scales with stiff hair teeth,

fronds are more densely paleaceous, with the im-
bricated scales completely obscuring the frond sur-
face. Furthermore, E. splendens has black scales on
the abaxial surface of the costa, which are absent
in E. splendens.

The following misapplied name found in the ear-
ly Mascarene literature should refer to E. splendens:
Acrostichum squamosum sensu Baker. Fl. Mauritius
512. 1877, sensu Cordem., Fl. Réunion, part 1: 85.
1891, Fl. Réunion 96. 1895, non Acrostichum squa-
mosum Sw., J. Bot. (Schrader) 1800(2): 11. 1801

—

анс MAURITIUS. Grand

76 (MAU,

Selected specimens
Bassin, Pétrin, Bijoux 7
plemousses in | N.
Rouhan & Grangaud 247 (NY. P, PT BG); Bébour, 11 10
Bassin = Hirondelles, Guého in MAU 15366 (MAU); Ci-
laos, sentier de la Mare à Joseph au coteau Kerveguen,
Badré 937 | (Р [2]); Cilaos, sentier GR RI entre “Le Bloc P
et le gîte de la Caverne Dufour, Rouhan = NY, P,
PTBG), Rouhan 218 (NY, P); Ci e de Salazie, N of Piton

Marmite, Lorence et al. 7544 (MO, PTBG); Cirque de! Sal-
але. Rouhan et al. 225 (Р, PT BG): Col de Bellevue.

Grande Montée de la Plaine des Cafres, Lorence 2463
(MO); Dimitile, Rouhan & Grangaud 203 (NY, P, PTBG);
"rand И Lorence in MAU 15631 (MAU), Staub in
MAU. 3012 (MAU); Hauts ane Saint- Jas З June 1882,
о Lilet Alcide, Rouhan E al. 243 (P); Montée
EN la Plaine des Palmistes, Bosser 9529 d 118 parte, left-
hand specimen]); Piton des Neiges, near le Gite, Lorence
in as 15650 A-C (M. un Plaine des Chicots, га de
. Vincent s.n. (P); Plait des ня res, Boivin 799 (Р);
Pipe е ben 109: 7 (MAU [244 1); а
len о (МО); s. loc.. Com-
2).

a

near Les Aviror

merson s.n. (P- T

2]. Elaphoglossum stipitatum (Bory ex Fée) T.
Moore, Index Fil.: 15. 1857. Acrostichum stip-
itatum Bory ex Fée, Mém. Foug., 2: 38, tab.
4(3). 1844 [1845]. TYPE: Bourbon [Réunion].
Salazie, s.d., s.n. Hb. Bory 27,12] (holotype,
Р!). Figure 3D.

Fronds spaced 0.5-1.5 em, borne in 2 ranks;
rhizome long-creeping, 1.5-2 mm diam., occasion-
ally branched, densely paleaceous; scales 3-5 X
0.4—0.6 mm,
reddish brown to blackish, paler basally, base cor-
date to sagittate, apex narrowly acuminate, sinuate,

narrowly ovate to linear-ovate, dark

filiform, margins bearing short, often paired hair
teeth, cells fusiform, in rows (Fig. 66). Phyllopodia
3-6 mm long, slightly swollen, dark brown; sterile
fronds 8-22(-44) cm; stipe 3-16(-25) cm, 0.5-1
mm diam., flexuous, stramineous to yellowish
brown, bearing numerous, spreading, rusty, narrow-
ly ovate scales 2-3 X 0.3-0.8 mm, base cordate to
auriculate, apex long-acute, slender, margins with
short hair teeth; brown resinous punctations also
present; blade oblong- to linear-ovate or oblong- to
linear-elliptic, 4.5-8(-19) X 0.9-1.5(-2) cm, base
cuneate to narrowly cuneate, shortly decurrent,
apex acute to obtuse, subcoriaceous to coriaceous,
costa prominulous and rounded abaxially, flattened
to shallowly canaliculate adaxially, both surfaces of
blade bearing spreading scales as in stipe, margins
thin, revolute, veins distinct, unbranched or 1 to 2
times bifurcate, apically free, adaxial surface thinly
covered with rusly to gray or white, narrowly ovate
0.2-0.3 mm long, base cordate t

-

scales 1—2
sagittate, apex slender, margins and basal lobes
bearing long, paired hair teeth, cells rectangular to
fusiform (Fig. 6H), abaxial surface glabrous except
costa bearing scattered scales like those on adaxial
surface of blade, both surfaces of blade bearing
short capitate trichomes and brown resinous punc-
ations. Fertile frond about equaling sterile frond;
stipe slender, 1.5 to 2.5 times longer than sterile
stipe; blade 5-7(-8.5) X 1-1.2(-1.4) cm, shape
and scales of adaxial surface as in sterile frond.
Spores 3840 X 25-30 pm (excluding perispore),

—

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

563

perispore cristate, crests 3—6 um high, margins
erose-dentate.

Distribution and habitat. Elaphoglossum stipi-

tatum is endemic to Réunion, where it occurs on
rocks or terrestrially in mats of bryophytes at 2000
to 2500 m, or in ericoid Philippia Klotzsch shrub-
lands.
Discussion. Elaphoglossum | stipitatum can be
distinguished by its sterile fronds with an adaxially
scaly, abaxially glabrous blade surface bearing
short capitate trichomes, and brown resinous punc-
tations. Furthermore, it is not epiphytic but occurs
at high elevations on rocks or terrestrially.
Elaphoglossum stipitatum is very closely allied
to or per haps conspecific with E. subcinnamomeum
(H. Christ)

Cameroon.

Hieron. from Kenya, Tanzania, and
Both species grow at high elevations
and exhibit short capitate trichomes in addition to
similar scale characters. Nevertheless, we refrain

from placing E. subcinnamomeum in synonymy un-
til more specimens of this species have been col-

lected and examined.

REUNIC ON. Cilaos, GR
la Caverne Dufour, Rou-
G. D

Selec ted A imens ar
RI x Bloc” et le gîte de
han . Р, PTBG); ee mea M. G. De
m s bis ( (Р [2]: Piton des Neiges, Lorence 407 (МО):
Plaine des ET Cadet 2048 (P); Salazie, s.n. Hb. 2
05 2| (P); Sommet 0 Grand Bénard, 16 Feb. 1847,

1 1847-1852 (P); Volcan, Pas de Bellecombe. Кашат &
Ganaan 221 (NY, P PTBG)

22. Elaphoglossum

tomentosum (Богу ex
Willd.) Н. Christ, Farnkr. Erde 37. 1897. Ac-
rostichum tomentosum Bory ex Willd., Sp. Pl

ed. 4, 5: 101. FOE TX PE: ^p. Ile de France"
[Mauritius]. J. B. С
s.n. [Hb. Bory 27.26] ем designated by
Rouhan & Lorence (2003: 840), PI). Figure

E.

Fronds caespitose, borne in 2 ranks; rhizome
short-creeping, 4 mm diam., occasionally branched.
moderately paleaceous; scales 1.5-3 X 0.25-0.5
mm, triangular to unguiculate, dull dark brown. ap-
pressed, persistent, base truncate to cordate, apex
acuminate, margins entire, scarious to erose, cells
opaque. Phyllopodia 8-10 mm long, slightly swol-
len, brown to dark brown, bearing scales as in rhi-
zome; sterile fronds 25—40(—50) em; stipe 4—8(-11)
.2— pale yellowish orange, сап-
aliculate, narrowly winged distally, when young
bearing numerous, dull brown, opaque elliptic to
unguiculate scales 1.5-2.5 mm long, 0.4-0.6 mm
wide, margins fimbriate, cells fusiform to irregularly
polygonal-rounded, thick-walled; blade linear-ob-
long, 20—40(—44) х 2-3(-4.6) cm, base cuneate to

cm, mm diam.,

narrowly cuneate to attenuate, apex acute to long-
acuminate, subcoriaceous, costa prominulous and
rounded abaxially, shallowly canaliculate adaxially,
yellowish orange, margins rounded, slightly revo-
lute, veins unbranched or bifurcate, tips apically
uniting into an intramarginal commissure, both sur-
faces of young blade covered by a thin but dense
layer of closely appressed, contiguous ovate to scu-
telliform, peltate scales 0.5-1 mm diam., pale
brown or gray with darker centers, margins fimbri-
ale. central cells square, marginal cells elongate

ig. OH), adaxial blade surface glabrescent. Fertile
frond 20-28(-38) cm long; stipe slender, as long as
or slightly exceeding sterile stipe: blade 13—19(—
23) X 0.9-1.3(-2.3) cm, narrowly elliptic to linear-
elliptic, base cuneate to attenuate, apex acute, ad-
axial surface bearing a dense layer of contiguous
23— a

p.m (excluding perispore), perispore cristate, 5—7.

scales as in sterile frond. Spores 35-38 X
pm high with finely erose-dentate margins.

endemic.
Wet forests from 300 to 900 m, growing epiphyti-
cally to 10 m above the ground, and occasionally
on boulders or terrestrially. Although three old col-
lections are said to be from Bourbon [Réunion], no

Distribution and habitat. Mauritius.

recent collections are known from that island.

Discussion. Elaphoglossum tomentosum resem-
bles E. heterolepis by the blade covered by a thin
continuous layer of appressed scales, but differs by
veins that unite apically into an intramarginal com-
missure, by its single type of laminar scales that
form a thin layer over the blade, and by the dull
brown. monochrome rhizome and stipe scales. On

Mauritius .

with E. heterolepis producing the nothospecies E.

tomentosum occasionally hybridizes

Xheterophlebium. It also hybridizes with the en-

demic E. lanatum producing E. Xadulterinum

1984).

The following misapplied name is very common

(Lorence,

in the literature for the Mascarene area: Elapho-
glossum (or Acrostichum) obductum sensu auct. (see
discussion under E. lancifolium).

M. 1 Alexan-
Roc et al. 178 (MAU, ‚ Р, PTBG); riis
'e. Lorence in MAU 1 1 5 (MAU):
Fer, Lorence 17.1 (MO); Crown Land Declerc,
); Gorges de la Riviére Noire,
| m 1092 (MO, Р); Le Pouce
15180 (MAU); bois de la partie supérie
Boivin s.n. (P); Macabé мм, Lorence 1303 (МО); Ма-
cabé, sentier е А Іа е aux Jones, Rouhan et al.
180 (MAU, NY, Р, PTBG); Mac abé-Brise Fer rd., Lorence
in MAU JA (MAU); Mare D Vaughan in MAU
10084 (MAU); Mt. Lagrave, E flank, Lorence 793 in MAU
18780 (MAU); Pétrin-Macabé rd., 1 MAU 14587
(MAU); Pétrin Nat. Reserve, Lorence 13.5 in MAU 15817

Selected. specimens examined.
dra Falls, R
Lorence 297
Crown Land Le Bouton,

564 Annals of the
Missouri Botanical Garden

(К, MAU, MO, P, REU); I 100 5 — in logical reconnaissance of Rodriguez Island, Indian
MAU 15011 (K, MAU, Р, REU); valley scade 500 Ocean. Nature 206: 26—27.
e Lorence 1166 (K, MO); valle; (dis MEM 500 . Mabberely, D. J. 1997. The Plant-Book, And ed. Cam-
"ieds, Lorence et al. 6990 (MAU, PTBG). RÉUNION. bridge Univ. Press, Cambridge.
79 in error], s.l., Habitat in insula Borboniae |Ré- Manton, 1. & W. A. Sledge. 1954. Observations on the
union], Bory de St. Vincent s.n. |legit. Flügge, in se à xd. |, cytology and о of the pteridophyte flora of Cey-
lon. Philos. Trans., Ser. B, 238: 127 -180.

a / OSs "oho "

P^ e : FEM к a Mickel, J. T. 2002. Elaphoglossum. Pp. 7-27 in H. J. Be-
entje ие Flora of Tropical East Afric ‘a, Lomariop-
sidaceae. A, Jalkema, irc Чат.

. " —— — & L. Ate hei. 1980. Subdivision of the genus

Literature Cited ШОЛ Amer. Ferr | 70: 47-68.

— — › >
Alston, A. Н. С. 1956. ~ subdivision of the Polypodi- Mexi & J. Beitel, 1988. 1 0 Hora s ше a,
арала. Taxon 5 23-25 exico. Mem. New York Bot. Gard. 48: 1-56 |
The Ferna aud Боен Абе of Wasi Thpt Moore, T. 1857-1862. Index Fili um: А syno s is, witl
cal Ме ^^ supplement to the second edition of the mu the 3 and an 5 ration of the
flora of West Tropical Africa. Crown Agents for Oversea dun ann WIID. SYNONYMES, ems sar LONE
Governments and Administrations, Millbank, London. M cor R. C. & R. Ril 1905 Elaphoel Pp. 250
Badré, F. & T. Cadet. 1978. er pteridophytes of Réunion penu 1 2: T e Knaor р.
Island. 3 i Ее 11: 349-365. in C. Dav idse, M. Sousa S. & p (editors),
Baker. J. G. Flora of Mauritius and the Seychelles: Flora Mesoameric ana, Vol | Unive 2 Nac ional Au-
London. tónoma de México, Mé xico, D. F.: Missouri Botanical

— W. 1837. Hortus Mauritianus. Port Louis, Mauri- шн St. Louis: The Natural History Museum, Lon-
aon.

Christ H. 1899. Monographie e A пиз Elaphoglossum. — —— & А. К. Smith. 2001. 5 relation-

Neue Denkschr. Allg. Schw Cea, Cesammten: Na- ships between neotropical and African-Madagascan pte-
dui Brittonia 53: 304-351.

turwiss. 36 ari 1 59. ;
Cordemoy, E. J. de. 1895. Flore de l'ile de la Réunion. Morton, C. V. 1965. IV. Proposals in p ea
Par polos Schott ex J. Smith. Regnum Veg. :
Crabbe; LA А.,

А. C. Jermy & J. T. Mickel. 1975. А new

1967. Studies of fern types, I. Contr. U.S. Natl.

eneric sequence for the pte a hyte herbarium. Fern
E п 141-162. pM BUS 28 20-83.
Fée, A. L. А. 1845. Mémoire sur les familles des fouge гез, Herb, .] He apum of fern types, II. Contr. U.S. Natl.
Deuxiè a mé moire: Histoire des Acrostichées. Ber 0-2
Levr u " ras sbourg = Бе Palmer, p. D. 2003. Hawaiis Ferns and Fern Allies. Univ.
4 є ri ›
Fishe coe & B. С. Heezen. 1907. Mas- Hawaii Press, с
сагепе ee western Indian У ean. Bull. Geol. Soc. Pichi Sermolli, R. E. 1968. Adumbratio de aethio-
Amer. 78: 1247-1266 picae. aplicar Me bia 23: 209-246.
Стешег: еШ FR Barrie. H. M. Burdet. Kou ‚Н. Lorence. 2003. On the eee m
De moulin. T. s. [rem DH. Nicolson. P € С ha wo Pod 'arene 3 (Lomariopsidaceae):
J. E. Skog, P. Trehane, N. J. Turland & D. L. awk 555 'rolepis (Fée) Т. Moore and E. tomentosum (Bory
| "hee Т 59. 7 04i
worth (editore): 2000. Inte ie d of tania ex reat Christ. Taxon 52: 837—840.
Nomenclature = Louis Code). Regnum Veg — ы fs Dubuisson, | N J. Motley,
E. 1977. A Monograph T e "ern 1 5 nus J. el, J.-N. Labat & R. C. Moran. Y 01. Molec-
s iiu ny of the fern genus 5 (Ela-

He 'nnipman, |
В‹ bit tis (Lomariopsidaceae) Leiden Botanical Series,
Vol. 2. Leiden Univ. Ss, Leiden

Kramer, K U. Р. r Green & A. Goetz. 1990. The Fam-
ilies and Genera of Vasc ular Plants, I. Pteridophytes
and UN Ed. K. Kubitzki. Springer-Verlag,
Berlin, New

Lorence, D. H. Я . Notes on some Mascarene speci
|

phoglossaceae) based on c hloroplast non-coding DNA
sequences: Contributions of species from the T0
Ocean area. Molec. Phylogenet. Evol. 33: 745-763.
Roux, J. P. 2001. Conspectus of Southern African Pteri-
dophyta. Southe dr African Botanical Diversity Network
Report No. 13. SABONET, Pretoria
Schelpe, E. A. C. - К. 1969. Revision 1 of tropic cal African

of a ia ae (Lomari psidaceae sensu Holttum),
Fer . 19 pteridophytes. 4. The ero ы eae of اوو‎
— boos The 2 E of Rodrigues Island. tropic = Africa. ne Bolus Herb. 1: 25— |
Bot. J. Г Soc. 72: 269-283. Se Ta ‚ М. 1834. Genera Filicum. Wallishausser, Vi-
——. 19 The pteridophytes of Mauritius (Indian
Ocean): Eeology and distribution. Bot. J. Linn. Soc. 76: Siedze, М. А. 1967. The genus Elaphoglossum in In-
201—241. dian ps а and Ceylon. Bull. Brit. Mus. (Nat. Hist.),
984. d in е а in the Bot. 4: 81—
1: 1-35 Smith, I. Um p? мүн and definition of the gen-

era of ferns, with observations on the 1 ^s E each
genus. J. Bot. (Hooke d 127): 38-70, 147—

Stalle su, F. A. & R. S. Cowan. 1976. e 13
A selective guide to botanical у ations "ut wi "c-

Masc gions a lane ern Gaz.
19 A monograph of {һе o (La
ales) i in Le Malagasy Re gion кн Indian Oc а,
Ann. Missouri Bot. Gard. 72: 1—10
9 B of Mas scarene Pterido-

phy ner. E Bot. (supplement) 79: 115. [Abstract.] tions with dates, commentaries and types. Vol.

Me Dougall, | & F. H. 1 1969. Isotopic dating Bohn. Scheltema & H H ema, Utrec
and geomagnetic polarity studies on ps volcanic rocks ardieu-Blot, M.-L. 1959. Sur les i NO de la
from 1 Indian Ocean. Bull. Geol. Soc. Amer. région malgac he avec е scription d'espèces nouvelles.
80: pe dre Notul. Syst. 15: 425-44:

i M & V. J. Wadsworth. 1965. A geo- ———. 1960. 5 (sensu lato). Blechnacées—

Volume 91, Number 4
2004

Lorence & Rouhan
Mascarene Elaphoglossum

Polypodiacées in Н. Humbert, Flore de Madagascar et
des Come = T lantes Mae о 5e Famille 2. Paris.
Trvon, R. M. . F. Try y
with Spec id Re im * Tropical Ame erica. Springe
gw n ч rk
Voss. К. аа е E ент У. ре moulin,
3 Mie Е Wi ү? Хеш, . Meikle, Н.
Rollins. P. € e va & W. С 1983.
nana Code of D» inical Nomenclature (Sydney
iode). Regnum Veg.
m W. Н. Ir. & К. E Che n. 1965. Abortion of
and sporangia as a tool in the detection of Dryoj
Amer. Fern J. 55: 9-29
"oS. Wagner & W Taylor. 1986. Detecting
abortive spores in Ad specimens of sterile hy-
140.

Amer. Fern J. 76: 129—

hybrids.

brids.
APPENDIX I. List of species and varieties.
. Elaphoglossum acrostichoides ie ы Grev.) Schelpe
Xadulterinum Loret
sum sh ey (Blume) T о
4. HI O ж auber ii (Desv.) Т.

9. Elaphoglossum hybridum (Bory) Brack.
Оа. Elaphoglossum hybridum (Bory) Brack. var. hybridum
Ob. El iphogloss ит hybridum var. vulcani (Lepervanche
ex Fée) Chris

10. Do un is (Bojer ex Baker) Lorence

11. е нм 5 (Desv. ) C. V. Morton

12. Elaphoglos epervanchet (Bory ex ha T Moore
13. а sid macropodium (Fée) я

14. а ssum Hide in Loren
15. Elaphoglossum ric 1 (Bory ex Fé T
16. Elaphoglos ssum 7 (Will E: ex Kuh n) C.
aac Lore
ieberi (Hook.

Christ
Chr.

21. Elaphoglossum stipitatum (Bory ex Fée)
22. Elaphoglossum tomentosum (Bory ex W illd. ) 3 c ‘hrist

APPENDIX 2. Index to exsiccatae.
The numbers in parentheses refer to the corresponding
I" les ee varieties in the text rn in Appendix l. Spec-
ed in alphabetic order by first collector. Col-
Neon ا‎ in boldface type indicate type speci-
nens

Badré 866 (1), 896 (7), 937 (20). 960 10 985 a
1004 (4), 1005 (9a); Bédier 51 (19), 7). 54
(13), 56 (15), 57 (15): 0 60 in м " ES a LT A
(13); Bo ivin [1847-18 52] (21), 799 (20), y ). 801 (1).
802 (13); Bosser 9529 (20), 9544 (4), 9559 (13), 9561

(19), 11857 (9a), 20432 (13), 20460 ( 0% 20624 (11),
21012 (6), 21503 (4), 21759 (4), 22485

Cadet 123 (4), 317 (13), i PN 1), ИТ 05 (1 ,
879 (15), 880 (7), 1535 (16), 1556 (3), 1556 (9а), 1702
(7), 1749 (1), 1778 (3), 19294 (U) 1930 (3). 1930 bis a.
2048 (21), 2063 (5), 3718 (11), 3766 (12), 3790 (1).
3884 (15), 4017 (12), 4028 (1), 4122 (1), 4126 (6), 4127

(11), 4130 (12); Coode 5007 (19).

De Lisle 82 (19), 396 bis (21); Des Abbayes 2950 (16);
01]

Du Petit-Thouars s.n. [18 (11), s.n. [1808] (4).

Edgerley s.n. in MAU 12464 (18).

Guého in MAU 11498 (9a), in MAU 11).
MAU 15362 (11), in MAU 15363 (19), in e 1536 0
(20).

Humbert 24918 (6).

Julien in MAU 13318 (12), in MAU 14585 (18), in

MAU 14594 (11), in MAU 14595 (9a), in MAU 15180
(22), in MAU 16494 (9a).
Lépervanche-Méziéres 14 (3); Lorence 2.2 (18), 2.3 in

MAU 15831 (1 2), 2.11 (7), 3.1 in MAU (12), FR6 in MAL
15618 (19), 7.3 in MAU 15813 (11), 8.5 (11), 8.6 in MAU
15531 (l A), 9.1 (18), 021 in „MAU 15814 (18). 103 (10)
‚ 12.1 in MAU 13.5 in MAU

ion in MAU P

2 in MAU (s (10), M129 (18). :

YW
z
ES
d
=

163 es 783 in

5 (11), 793 in MAU
18780 (22), 828 in MAU 16319 EN 847 (2), fn (18),
| 16518 (8), 1074 (18), 107 8 (7). 2

—
~
T
~
^
ч

1544. (8), 1608 (9a), 1609 (2). 1610 (2), 1626
(12). 2163 ( 20), 2496 (9b), 2520 (1). 6944: (9a), 6990 (22),
7017 (11), 4 (20), 75 ap (6), in MAU 1458
MAU I 1586 (18). in MAU 14587 (22). in M.
in MAU 14589 (12), in Ten 14599 (7),
(22). in MAU 14605 (22), in MAU 14609 (2,
14610 (12), in MAU 14640 (12), in MAU 14

MAU 15010 (12), in MAU 15011 (22), in MAU 15016
in MAU 15024 (9a), in MAU 15099 (8), in MAU
(12), in MAU 15243 (10), in же 15533 (10), in Tm
in MAU pi эм AU 15615 (3). in MAU
3. in MAU 15621 (1). in MAU

in MAU
380 (12). in
2

; 9 à)
15631 (20), in ve 15637 (п), І
15040 (3), in MAU TE (12), in MAL
in MAU 15645 (7), in MAU 15647 (15), in М,
(1). in MAU 15650 A-C (20), in MAU 15810 (7)
15823 (10), in MAU 15823a (9a), in MAU 158 bibas ).
in MAU 16018 (7), in MAU 16019 (7). in MAU 16307 (2).
in MAU 18785 (7).

Richard 10 (15); Rouhan 169 (18), 175 (12). 177 (1).
178 (22), 179 (7), 180 (22), 181 (11), tS (11), Td
190 (14), 192 (10). 193 (11). 194 (10), E (9a). 197 (11).
198 (9a), 199 (6), 201 . 202 (7),
205 (15), 206 (4), 207 (13), 208 (12). ad (13), 210 (11),
211 (7), 212 (21), 213 (20). 214 nh. 215 (1). 4
(9a), 218 (20), p (9b), 220 (3), 2 22
224 (16), 225 (20), 226 (4), F (12), 2
231 (15), 232 (13), 233 (3), 234 (15), icy 19), 236 (11),
239 (9a), 241 (4), 242 (1), 8 Bo! 244 i 5), 246 (19),
247 (20), 248 (12), 249 (1), 250 (9a).

10849 20), е in MAU 12416 (11).
10934 1 (2X ieber Flora Mixta 281 (7)
Staub in MAU 11348 CUR in MAU 13012 (20).

Vaughan in MAU 2500 (18), in MAU 10084. (22), in
MAL 125 44 (11). in MAU 12551 (12). in MAU 12593
(18), in MAU 12624 (18).

Wiehe 1721 (3).

Schlieben

10954. (7),

Frederic Lens, * Kathleen A. Kron,”
James L. Luteyn, Erik Smets,? and
Steven Jansen?”

COMPARATIVE WOOD
ANATOMY OF THE
BLUEBERRY TRIBE
(VACCINIEAE, ERICACEAE
S.L.)!

ABSTRACT

Wood samples of 111 Vaccinieae specimens (Vaccinioideae, Ericaceae s.l.) representing 98 species and 26 genera
are investigated with light microscopy and scanning electron microscopy. The wood structure of Vaccinieae delivers
taxonomically important characters that can be used to define some subclades within the tribe. The wood of the large
polyphyletic genus Vaccinium strongly resembles non-vaccinioid members of the family, which are characterized by
bordered vessel-ray pits and relatively narrow (2- to 4-se riate) and low еш 17920 rays Gy en Pen than 1000 jum) with
exclusively or mainly procumbent body ray cells. The East Malesian clade, ibbean clade, and the
Andean clade show a combination of wood anatomic alf hna that is lacking in other re eden of the family.
These features include scalariform vessel-ray pits with strongly reduced borders, a high portion of upright body ray

Meso-American

cells, wide
ray cells (although absent in |
pith tissue may represent a d i
chyma cells, usually ranging from 500

Key words:

(A- to 14-seriate) and high mu iltiseriate rays (often more than 3000 um), and prismatic c crystals
оаа racemosa). The presence of s

in chambered

secretory ducts in the primary xylem and in the

the Andean clade. Furthermore, the presence of undivided axial paren-
) рт. seems to be unique in the subfamily.
blueberries, онна rie anatomy, Ericaceae, Neotropics, secretory ducts, systematics, Vaccinieae.

The tribe Vaccinieae Rchb. (Ericaceae Juss. s.l.)
comprises about 35 genera and more than 1000
species. Most representatives are evergreen shrubs,
many occurring as epiphytes and occasionally as
lianas. The vast majority of the taxa (about 30 gen-
era and 900 species) are concentrated in the cooler.
moist, montane areas of South America between
1500 and 3000 m (Luteyn, 2002). The remaining
laxa are concentrated

—

southeast Asia and Malesia, and a few species are
restricted to southeast Africa and Madagascar. Vac-
cinium L., the only genus that occurs in the tropics
of the Old and New World.
the tribe (ca. 450 species), but it does not seem to
be monophyletic according to molecular data (Kron
et al., 2002b).

Hooker (1876) considered the blueberry tribe as
a separate family, Vacciniaceae Gray, particularly
because of the inferior ovary and the fleshy fruit.

in the montane regions of

is by far the largest of

Based on the overwhelming similarities between
Vacciniaceae and Ericaceae, most authors placed
the study group as a tribe within the subfamily Vac-
cinioideae Arn. of the Ericaceae (Drude, 1897; Ste-
vens, 1971). In the classification of Stevens (1971),
the circumscription of Vaccinioideae was greatly
enlarged by the inclusion of Arbuteae Meisn., An-
dromedeae Klotzsch, Cassiopeae P. F. Stevens, and
Enkiantheae P. F. Stevens. In the most recent clas-
sification of Kron et al. (2002a), based on molecular
as well as morphological data, Vaccinieae are sister
to Andromedeae s. str. and Gaultherieae Nied.,
which form together with Lyonieae Kron & Judd
and Oxydendreae Н. Т. Cox the rest of the subfam-
ily Vaccinioideae.

Within the study group, the systematic relation-
ships are far from resolved. Many earlier botanists
divided Vacciniaceae into two tribes, namely Vac-
& Hook.f.,

cinieae and Thibaudieae Benth. based

! The directors of the!

of the wood collections of Leiden, Kew, Maddis

Fund for Scientific Resear

Laboratory of Plant S

—Vlaande теп) (G.104.01,

systematics, Institute of Botany and Моор, K.U

National Botanic es n E Belgium, the Royal Botanic Gardens of Edinburgh, and the curators
, Utrecht, and Tervuren are greatly acknowledged for use ir supply of
wood samples. Special thanks to Dr. Wallace (Rane ho Santa Ana Botanic Garder
Anja Vandeperre (K.U.Leuven) for technical assistance and
SEM micrographs. This work has been supported by
ch—Flanders (F.W.O.

Jansen i is a postdoctoral fellow of the Fund for Scientific Resea

1) for sending wood materi e thank
Marcel Verhaegen (National Holame 1 Garder of Belgium)
research grants of the Leuven (OT/01/
1.5.069.02, l. 5.061.03). Steven
rch—Flanders (Belgium) (F.W.O.—V laanderen)
euven, Kasteelpark Arenberg 31, B-

3001 Leuven, Belgium. frederic.lens@bio.kuleuven.ae.be (author for сөзү aie

M ۰ nt of Biology, Wake Forest University,
Ne York Botanical Garden, Bronx,
5 Res al Botanic Kew,

New York
Gardens.

ANN. MissoURI Bor. GARD. 9l:

Winston- Salem, N ie
10458-5126,
Richmond, Surrey TW9 308. United | ae

566—592. 2004.

Carolina 21 109-7325, U.S.A.

Volume 91, Number 4

Lens et al.
Wood Anatomy of Vaccinieae

on flower morphology and leaf anatomy (Hooker,
1876: Niedenzu. 1890: Drude, 1897). Nevertheless.
the two tribes could not be clearly distinguished
from each other because of the variation in the flow-
ers and leaves of some genera. Also the generic
boundaries within the study group, traditionally
seed, and vegetative char-

based on flower, fruit,

acters, caused many problems (Sleumer, 1941: Lu-
1991).

nieae has increased significantly. although several

teyn, Nowadays, our knowledge of Vacci-
genera still remain poorly studied (Stevens. 1985).

This can be illustrated, for instance. by molecular
sequence data, which show that only few Vacci-
nieae genera seem to be monophyletic (Kron et al..
2002b). On the other hand, five major evolutionary
lines within Vaccinieae could be established. i.e..
a large Andean clade with the majority of genera.
Mal-

esian clade, an Agapetes G. Don clade with some

a Meso-American/Caribbean clade, an East
Asian Vaccinium and Agapetes species, and a Vac-
cintum clade with members of Vaccinium sections
Bracteata and Oarianthe.

The wood anatomy of the blueberry tribe is only
Metcalfe and Chalk (1950)

commented on the wood anatomy of a few species

fragmentarily known.
of Agapetes, Gaylussacia Kunth, Macleania Hook..
Paphia Seem.. Psammisia Klotzsch, and Vaccin-
tum. Other authors investigated the secondary xv-
lem of several species belonging to only one genus.
Giebel (1983) studied the wood anat-
Lindl., Noshiro

(1988) investigated Agapetes, and species of Vac-

For instance.

omy of Cavendishia Suzuki and

—

cinium were treated by, for instance, Flint (1918
Moll and Janssonius (1926), Greguss (1959), Wein-
gartner (1969). Baas (1979), Carlquist (1985.
1988), Odell et al. (1989), Queiroz and Der
Burgh (1989), Stuzková et al. (2003). and Edwards
and Axe (2004).

This work aims to present a detailed wood ana-
tomical overview of the tribe Vaccinieae, including
most genera except for Anthopteropsis A. С. Sm..
Costera J. J. Sm..
ocalyx Planch. & Lindl.,

Didonica Luteyn & Wilbur. Gon-
Paphia, Pellegrinia Sleu-
mer, Rusbya Britton, and Utleya Wilbur & Luteyn.
Special emphasis is paid to comparison of the wood
anatomical variation with recent taxonomic insights
based on molecular sequence data in order to re-
veal possible evolutionary patterns and to look for
wood anatomical support in one or more evolution-
ary lines. The presence of fibers with a living pro-
toplast, as has been discovered previously by sev-
eral authors in Vaccinioideae (Braun, 1961; Fahn
& Leshem, 1962: Giebel, 1983; Lens et al., 2004a),
will also be discussed briefly. This manuscript is
part of a general wood anatomical survey of Vac-

2004a). '
anatomy of the subfamily is treated elsewhere (Lens

2004b).

cinioideae (Lens et al.. Phe ecological wood

et al..

MATERIAL AND METHODS

Wood samples of 111 specimens representing 98
species and 26 genera (cf. Index, Table 1) were
investigated using light microscopy (LM) and scan-
ning electron microscopy (SEM). For LM observa-
tions, transverse and longitudinal sections of about
25 pm were cut using a sledge microtome (Reich-
ert, Vienna, Austria), after softening the wood sam-
ples in hot water: a previous warming of the knives
is not necessary. Transverse sections of tiny sam-
ples were cut using two pieces of polystyrene foam.
In order to make tangential and radial longitudinal
sections of these thin stems, the sample was mount-
ed with superglue on a rectangular piece of wood
that was clamped in the microtome holder. The en-
tire thickness of the wood sample could then be
used to produce longitudinal sections. All the sec-
tions were bleached with sodium hypochlorite and
stained with a mixture of safranin and alcian blue
(35:65). The safranin was prepared as a 1% solu-
tion in 50% ethanol, while the 1% alcian blue stain
was dissolved in pure water. Afterward,
were dehydrated with 50%-75%—96% ethanol and

mounted in Euparal. LM observations were carried

the tissues

oul using a Dialux 20 light microscope (Leitz, Wet-
лаг. Germany), and pictures were taken using a
DP50-CU digital camera (Olympus. Hamburg, Ger-
many). Preparations for macerations were made us-
ing a hot mixture of glacial acetic acid and hydro-

(Franklin. SEM

observations, wood samples were softened in hot

gen peroxide 9045). For

water, Longitudinal wood sections were made using
The sections were bleached with so-
50%-

the sections were

a razor blade.
dium hypochlorite and dehydrated with
5% 00% ethanol. Afterward.
gold-coated with a sputter coater (SPI Supplies.
West Chester, Pennsylvania, U.S.A.) and observed
using a JEOL JSM-5800 LV scanning electron mi-
croscope (JEOL Ltd.,

uated in the National Botanic (

Tokyo, Japan), which is sit-
sarden of Belgium.
The wood anatomical terminology follows the
“TAWA list of microscopic features for hardwood

" (IAWA Committee, 1989).

of the difficulties in determining the type of non-

identification Because
perforated tracheary elements, a description is giv-
en below.

All types of non-perforated tracheary elements.
i.e., tracheids, fiber-tracheids, and libriform fibers,
the wood of Ericaceae s.l. (Baas.

2003).

e present

I
1979; Carlquist, 1988; Lens et al.,

It may

568 Annals of the
Missouri Botanical Garden

Table 1. Survey of selected wood anatomical features within Vaccinieae. + = present, = = absent, + = sometimes

resent, ? = unknown. ^^" Numbers after the names of specimens refer to the order used in the material list. Minimum

and maximum values are shown in parentheses. “>” means that the height of the multiseriate ray exceeds the length
of the section.

Vessels
Helical
Percent- thicken- Helical
Secretory age of Sealari- Alter- ing thicken-
ducts in scalari- edo form nate ик through- ings Tangential
pith or form sel- vessel- vessel- vessel- out in fibers diameter of
primary perfora- Number ray ray vessel and/or vessel lumina Vessels pe
Species studied xylem tions of bars amine cine pitting pitting elements. tracheids (jum) square mm
Agapetes flava — 10 (1-)4(-6) + — 4 = + — (42 018025) (210-)288(-390)
А. hosseana = 100 (7—14(-24) + — + — = — (10-)18(— 2 (140—)194(—240)
A. mannii = 100 (6-)9(-11) * = + = + + (10—)15(—18) (300-)379(—440)
A. moorei = 85 (2-)99(-15) + = + = = = (1 Eus 22) (120-)145(-200)
A, sikkimensis = 20 (2-)8(-13) + = T = = = (19-)25(-30) (140—)169(-200)
А. variegata = 20 (7—)10(—12) + " + — = = (20-)26(-35) (96-)122(-160)
Anthopterus
wardit! ? 100 (8—12(-20) + + — + = = (15-)20(-30) 02 129-178)
А. зага? + 90 (13715) + + = + = = (25-)31(-50) (156-)190(-231)
Cavendishia
bracteata аз 70 (1359) = + = + = = (25-)37(-50) (70-)93(- 120)
C. duidae ? 25 (1338) ze + Е + = — (22-)29(-35) (140—)166(—192)
C. compacta E 60 (23549) = + — T = = (30-)39(-50) (126-)155(-178)
C. lindauiana + 90 (2-)5(-7) = + = + 2 = (25339250) (92—)111(—135)
C. pubescens ? 100 (2—)8(-12) = + = + = = (35—)47(—60) (36-)44(-58)
C. urophylla ? 70 (3-)5(-8) = + = + — = (2033040) (100—)126(—142)
Ceratostema ? 95 (2-)5(-7) Е + — + = = (20-)27(—40) (54—)91(—122)
reginaldit'
С. reginaldi ? 100 ()9%-13) - + - + + - (20—)28(—35) (32-)51(-95)
Demosthenesia
spectabilis + 100 (2-)5(-1) + + — + — = (45-925 32) (160—)178(-210)
Dimorphanth- ? 10 3-4 + + — + — — (110-163 (10-)18(-24)
era collinsii (-220)
D. cornuta var. 0 0 — 4 — + — = (60-103 (22-)21(-32)
cornuta (140)
D. dekockii ? 0 0 = + — + = — (60—)1 10 (16-)24(-32)
var. pubiflo- (-160)
D. kemptert- ? 10 9-10 + + — + — — (410-0164 (8—)12(—18)
апа (—205)
Diogenesia — 95 (1-)9(-15) — + — + — = (20-930 (40) (66-)95(-114)
floribunda
D. tetrandra + 80 (2-)7(-18) = + = + = = (20-)27(—40) (61-)73(—82)
Disterigma
sp. indet.! = 100 (6—510(-16) + + = = + + (12317(225) (240-)362(-415)
D. sp. indet.? ? 100 (4—12(-25) + + = — + + (12-)17(-20) (168-)223(-272)
D. alaterno- — 70 (1238417) = + = + — == (2533545) (70-)91(—120)
ides
D. cryptocalyx — 90 (1-)5(-9) Е + = s — — (4522025) (120 1528180)

Gaylussacia

baccata - 90 (2—)7(-12) : + + = (10-)116(-22) (215-)307(-370)

zx

d
||
+

piens = 90 (1—-)6(-10)

—

T — + + = (1532030) (23027 1(-362

—

Volume 91, Number 4 Lens et al. 569
2004 Wood Anatomy of Vaccinieae
Table |. Extended.
Rays
Multi Crystals
Vessels Tracheids Fibers seriate Present
ray width in axial

Length of vessel
elements (um)

Length of tracheids
(дт)

Length of fiber
tracheids (um)

(number

of cells)

Height of uniseriate
rays (jum)

Height of multiseriate
rays (jum)

Present paren-

in rays. chyma

(370-)472(-580)
(350—)548(—700)
(330—437(—550)
(370-)579(-740)
(460—)765(-940)

(530-)704(-840)

(450-)596(=
(480-)613(

150)
-770)

(390—)598(—750)
(450-)645(-870)

(450)635(-830)

(350-)529(-690)
(550-54
(1000)

(400—)560(—700)

(120-)608(-790)

(700-)930
(-1150)

(420-)684(-820)

(350-)548(-750

—

(250—)364(—550)

p (4: 2n)
(400—)72

E A

(1250)

280903030500)

2304000000)

(380—)437(—480)
(430—)532(-610)
(350—)481(—570)

(570-)638(—680)
(670—)805(—900)

(670—)740(—810)

(460—)576(—9300)
(550—)6 19(-690)

(570—)645(—720)
(600—)645(—700)
(600—753(—950)

(690-)734(-770
(560—)656(—85(

Л
м

(670-)730(-820)

(580-3093
(1000)

180-)530(-670)

(450—)619(—750)
(30001016
1200

(550008607280

(630-)823(-970)

(1100-)1396
(1600)

(640—)728(—820)
(500—)608(—700)
(350—)463(—0640)
ا‎ )460(—580)
— 7520-000)
E Jo090(—900)

NS

320—)375(—430)

—

==

320—)478(—050)

(480—)580(—640)
(620—)724(-910)

520-)634(-750)
700-)783(-970)

(880—)937(—1070)

(600—)829(— I 000)
(680—)823(—930)

(690—)94 1—1150)
(670—)833(-970)
(640—)892(—1150)
(650-)802(-920)
(900) 1060
(-1320)

(750-)956(-1140)
(770-)921(—1 100)

pm

680—)995(—1 160)

(560—)695(—520)

(6820—)990(— 1 120)

(800—)090(— 1 200)
(720—)889(—1050)
(600—)790(—950)
(400—)565(—750)
(400—)502(—650)
(700—)938(—1050)
(1120-)1252

(-1880)

(440—)500(—020)

(560—)688(—960)

3-15
1—5
6-9
6-12
5-11

6-10

+

(280-)459(-790)
(400-)739(-1300
(600-)850(-1204

(450—)744(-1000
(150-)993(-1600

—

)
)
)
)

(650—)1 766
(-3500)

(000-)936(-1800)
(450) 1
(22700)

(250-)577(-1300)
(300-)592(-950)
(300-)600(-950)
(350-)600(-800)
(550-)744(-850)

(200—)450(—1000)
(400—)763(—-1400)

(350-)807(-1400)

(150-)735(-1200)
(300-)605(-1200)

(200—)406(—550)

(300—)492(—950)

(300—)804(—1300)

(500—)1122

(-1750
(350—)780(—1400)
(200—)416(—650)
(200—)365(—650)
(400—)500(—650)
(600—)2357

(—5 100)

(650—)789(-1000)

(350—)572(-850)

—

1300—)2816(—1600)
950-)1327(-2150)
(1100—)1689(—3900)
1500-8500
711500

—

(2400-)3280(-4600)

>6000
>8000

De ups 3(—3000)

(1200-)2036(-2400)

(800—)1473(-2200)
(1100—)2605(—5500)

(900—)1569(—2 700)

(1600—)2267(—3500)
(7000—)8100(—9500)

(800-)2086(-3600)

(1800—)2843(—5000)

.

(4000-)6050(-8400)
>9200
(800-)3920(-6000)
(500—)643(-1000)
(400-) )693(- 1000)

900-> 5000
a m

(800—)1520(—3500)

(2100—)1963(—2700)

+

+

570

Annals of the
Missouri Botanical Garden

Table 1. Continued.
Vessels
Helical
Percent- thicken- Helical
Secretory age of Sealari- Alter- ing thicken
ducts in scalari- Өрройе- form nate Simpe through- ings Tangential
pith « г forn vessel- vessel- vessel- vessel- ou in fibers diameter of
primary perfora- Number ray \ гау ау vessel and/or vessel lumina Vessels per
Species studied ge m lions of bars pitting и pitting Em elements. tracheids (шт) square mm
Lateropora
ovata + 100 (5-10(-17) = + = + = = (15-)23(-30) (148-)194(-220)
Macleania Y 10 | (2-)5(-9) — + — + = = (35-)49(-60) (32-)54(-80)
crassa
М. ericae + 85 (2-)5(-9) = + = + = = (20—)29(—40) (90—)110(—130)
M. hirtiflora + 95 (2-)7(-13) — + — + — — (20-)26(-30) (83 0108-148)
\/. loeseneri- ? 90 (3-)7(-10) = + — T = = (20—)33(—50) | (48—)69(—90)
ana
M. pentaptera 2 0 0 — + — + — — (27333440) 32 058-98)
M. rupestris ? 0 0 - + — + — — (25—)51(—75) (44—)55(-08)
V. stricta E 45 (2-)6(-10) — + — + = = (25—)34(—40) (91—)105(—123)
Mycerinus chi- = 100 (1—)5(-7) — E — + — — (2032535) (105-)132(-160)
mantensis
Votopora
cardonae = 15 (3—)6(—11) = + — + — — (352) 45-00) (68-085 105)
N. schomburg-
ҮП — 0 0 — + = + — = (30—)46(—65) (40-0010)
Oreanthes ecu-
adorensis + 100 (3—)6(—12) = + — + — — (20-)26(-30) (180-)250(-290)
Orthaea fim-
briata + 80 (2-)6(-13) — + — + ~ E (20-)31(—40) (51—)62(—78)
Plutarchia
ecuadoren-
515 = 100 (3—)4(-6) = + = + = = (15-)20(-35) (430 145,172)
P. rigida = 95 (2-)4(-6) — + = + = x (20-)25(-30) (120—)146(-170)
Polyclita tur-
binata + 25 (1-)3(-6) = + = + = B (25-)28(-40) (81—)96(-120)
Psammisia sp. ? 0 0 — + — + — — 5-)85 (2433340)
indet. (-120)
P. ecuadorensis + 75 —)5(-8) = + = + = — (25-)38(-55) (53-)74(-90)
P. ferruginea ? 25 (3-)8(-13) = + = + = = (50373 (34—41(-52)
(120)
P. graebneri- + 95 (1-)7(-14) — + = + — = (15-)20(-35) (83-)97(-110)
ana
P. guianenis + 20 (8310-15) — + "a + = = (25-)37(-60) (60—)72(—90)
Р. guianensis + 85 (1-)8(-13) + + = + = — (25-)42(-65) (58-)79(-100)
P. penduliflora + 100 (3-)4(-9) — + — + — — . (20-)31(-40) (80—)997(-118)
P. cf. ulbrichi- + 50 (13715) — + = + = = (30-)50(-70) (32—)42(—50)
апа
Satyria sp
indet.! ? 95 (1235410) - + = + — — (28—)41(-00) (34—)52(—60)
S. sp. indet? ? 0 0 — + — B — — (65-)93 (22-)20(-32)

(-115)

Volume 91, Number 4 Lens et al. 571
2004 Wood Anatomy of Vaccinieae
Table l. Extended. Continued.
Rays
Crystals
Multi- Е
Vessels Tracheids Fibers seriate Present
ray width in axial
gth of vessel Length of tracheids Length of fiber (number Height of uniseriate Height of multiseriate Present paren-
e pr ments (am) (um) tracheids (jum) of cells) rays (jum) rays (um) rays chyma

(430-)567(-670) (520—)577(—620
(560—)795(-920) (670-844
(160—)653(—750)
(340-)586(-830) (
6

03055750)
(400—)617(—800) 50

9675-940)

(270—)551(-770) (4405205600)

gratie (910—)1 109
—1000) (-1340

(: Ока 30(—040) | (520—)590(—650)

(430—)697(—500) (2060—)678(—150)

(500—)697(—940) | (000—)648(—750)

(520—)700(—900) | (550—)725(—850)

(420—)649(—979) | (520—)580(—0670)

—

(550-)080/-850) (540 074500880)

(390-)558(-070)
(400-)556
(810)

(150—)480(—520)
(450—)519(—600)

(320—)561(—780) | (500—)664(—750)
(5380—)726(—880) (750-9038
(-1050)

(520-)69 44-870) | (650—)740(—850)
(020-)748(-930) (730—)871
(-1120)

(340579770) (470—)595(-700)
(7 eae (650—-)939
-]15 (-1150)

E РТИ (570—)650(—740)

(440—)630(—810) |. (580—)639(—680)

(500-0668800) | (700—)777(-870)

(500-)612(-820)
(750-)913
(-1100)

(470—)680(—850)
(450—)684(-870)

(620—)819(—920)
(970—)1 117
(—1290)
(890—) 1012
(—1 150)
850—)974(—11 70)
800—)994(— 1200)

(530—)789(— 1060)

(830-)928(-1020)

(720—)864(—1000)

(580—)862(—1 100)
(750—)925(—1250)
(540—)743(—1040)

(700—)979(—1 250)

(600—)716(—850)
(550—)749(-860)

(650—)760(—980)

(750-)1095
(-1230)

(840-)981(-1260)
70-)1146

(-1380)
(600-)844(-1060)
(11 5001 280

(1650)
(8: 10-)995(-1 170)

—

630—)815(—980)

(850—)1005
(-1170)

(720-)967(-1170)

(780-)999(-1170)

1-6 | (550-)950(-1550) 28000

4—5 Еген 1300->7300
(-17

(500— " VN JO)

—5 (550-)821(-1750) 4900->12000
З

(300—)446(—1200) (800—)1645(-3500)

1-7 9055 J860(- 1300) (1050—)1628(—1950)

3600-2 10500

2—3 (550-)1063
(—1900)

—— (550-)983(-1350) 2250-8000

I-5 (350-350-1800) (600022080

—

(450 0700 (1300) 28500

1-5 (350 0700-000) (1100-03485

400 94830550) 2500
1 665091350 5700
2000)

6— (500—)729(-1050) (1350-)2908(-4950)

3-4 | (250—)600(-1000) 500-4000

мї

3-5 (300—)900(-1500) 1400-28000
4-6 (400-)745(-1100) 5900-2 10.000

4-7 (620-2478 52008600
(-2100) (-10800
3-4 (250-)696(-1300) 2100-6000

6-8 (150-1710 713500
(1100)

1-5 (1350-)1583 8700-> 16500
(-2000)

3-4 (700-)1122 711000
(-1700)

5-6 (500—)740(-1100) 30008700

1-7 (400—)771(-1500) (1150-)2771(-5300)

(1100—)2343(—3400)

(1800—)4760(—7200)

(950—)1 704(—3200)

—3000)

3500)

d

—

4

+ +

572

Annals of the
Missouri Botanical Garden

Table 1. Continued.
Vessels
Helical
Percent- thicken- Helical
Secretory ge of Sealari- Alter- ing thicken
ducts in see 1 ari- Opposite form nate Simple through- ings Tangential
pith or form vessel- vessel- vessel- se oul in fibers diameter of
primary perfora- Number ray r ray ssel and/or vessel lumina Vessels per
Species studied xylem ions of bars pitting rian pining pitting elements tracheids (um) square mm
S. sp. indet.” ? 0 0 — + — + — — (60—)81 (40—)49(—08)
(100)
S. sp. indet.' Tt 40 (1-)5(-9) B T E + = = (30—40(—50) (66—)87(—120)
S. carnosiflora + 20 (2—)5(—11) = + = + = — (30-41(-60) (59—)79(—110)
S. meiantha ? 15 (2-)4(-0) = + — t — = . (30-)49(-60) (50-)02(-82)
S. panurensts ? 0 0 + + — + — = (60-0 (24—)28(-30)
(-140)
S. warszewiczit + 25 (3—)5(—8) — + — + — — (2033540) (81-)121(-167)
S. warszewiczit + 70 (2-)6(-11) = + = + — — (30-)37(-45) (32 005 100)
Semiramista 100 (7—)10(—15) + + = + = — (14—)21(—27) (87—)95(-105)
cherrima
Siphonandra ? 20 3-4 — + = + — — (25-)36(-50) (74 ) 80-108)
elliptica
Sphyrosper-
mum sp
indet. = 95 (2-)9(-20) = + — + — = (15-)19(-22) (180-)249(-320)
S. a — 100 (83106412) + + — + = — (20-)26(-31) (240-9318360)
S. sodiroi — 100 (8—11(-14) = + — + — = (11—)16(—25)
Symp ra- — 90 (9313-20) — + — + — — (2033340) (95-)103(-114)
cen
Themistoc lesia + 100 (73136416) —] + — + — — (25-)30(—35) (120—)153(-170)
epiphytica
T. pendula + 0 0 — + — + — — (30-)61(-85) (62-)75(-102)
T. vegasana T 20 (1-7(-11) + — + — — (159030045) (130—)156(-192)
Thibaudia an- + 95 (1-4(-9) ate + = + — — (20-)31(-40) (125—)159(-230)
gustifolia
T. floribunda + 30 )6(—13) — + = + — — . (20-)36(-45) (42-)64(-80)
T. formosa ? 90 (1-9) 7(-11) = + — + — — (20-034 55) (38—)70(-110)
T. jahnii + 90 (123610) — + — * — — (203545) (76—)107(—141)
T. martiniana 7 100 (4—)8(—10) — + — B — — (40—)53(-70) (36-)09(-84)
T. pachypoda + 35 (1-)A(-8) = + — + — — 630-9430 50) (100—)144(-185)
T. parvifolia ? 95 (13711) = + — + = = (20-)25(-30) (112-)141(-168)
T. rigidiflora ? 95 (135413) — + — + — — (30—)43(-60) (64—)81(—100)
Vaccinium sp. ? 50 (128418) ge + — — + — (15—)23(-40) (160—)228(-280)
indet.
V. africanum ? 75 (1-)8(-20) + + — + + — (25-)32(-40) 905 1388170)
V. angustifo- — 80 (1—)8(—12) + + + — + — (12-)18(229) (200-)267(-310)
ium
V. arboreum ? 75 (7-)26(-53) + + + — + + (18—)25(—40) (89—)109(—150)
V. atrococcum ? 85 (4310416) + + + $ + — (15-)23(-35) 3 240)
V. bancanum ? 0 0 + + + — — = (352046060) (52 0650-88)

Volume 91, Number 4

Lens et al.
Wood Anatomy of Vaccinieae

573

Table 1. Extended. Continued.
Rays
Multi- —
Vessels Tracheids Fibers seriate Present
ray width n axial
Length of vessel Length of tracheids Length of fiber (number Height of uniseriate Height of multiseriate Present paren-
elements (шт) (Am) tracheids (шт) of cells) rays (jum) rays (jum) in rays chyma
(580-)833(1080) (850 01069 (990—)1 146 I-7 (400—5)711(-1200) 1600 6000 + =
(-1190) (1300)
(420—)637(-900) (460 ) 7130-780) (850-1000 3—4 (250-)764(-1300) (1300-)2793(-5400) — =
(1180)
300205220650) (400 )5 43-660) (600) 740-9000) 3 (250—)485(—90) (800—)2845(—7000) T =
(490—)744(-990) (65090756350) (9001150 6 (350-)644(-1200) 1900-9000 7
(1500)
(640-0789 (840-038 (800-1053 9-14 (150—)881(—-1500) 2700- 12000 + —
(1000) (1100) (-1260)
(570745930) (630758810) (870 01004 1-8 (300—)647(-1450) 4000->11000 — ==
(1210)
(430-688-800) (620 07110800) (780 0010-1250) | 5-8 (400-700-1600) (1900-02600 3300) + —
(430 0640-380) (620-0685 740) (800—912(-1000) 1-5 (100-)1456 (1450-)2983(-3950) — =
—1200
(270—)430(—510) | (450—)546(-730) |(500—)662(—810) 7 (200-)466(-900) | (600—)1013(—1950) = =
(370-)512(-600) (390-477(-570) (540-)707(930) / 3 (150-)883(-1500) 1100->4100 B >
(340—)452(-600) (370—)457(-550) (450-0580070) o0 (150—)402(-600) (1200—-)1668(-2300) — =
(400—)620(-800) (400—)442(—520) |(630—)778(—-950) 2—4 (250-)444(-000) ? = —
(420 0620-850) (430-)508(—650) (800) 1010 | (350—)564(—900) |. (600—)1511(—2400) = =
(—1 150)
(180-)696(-890) |(560—)648(-720) (720—)880(-1050) — 1-12 (900—) 1400 210.000 = —
(1800
(280—)473(-730) (520 )594 (720) (650-)82 1(-930) 5-7 (1005352850) 1500—1900 + +
(400-)538(—650) (480—)593(—720) |(600—)766(—950) 3—5 (300—)538(-1100) 2400->6000 + ==
(570-)733(—930) |(600—)702) (180—)881(-1050) 3-5 (700—)1459 (1200—)3350(-0300) — =
(—780) (3000)
(410 9050806680) (570-163 7(-090) (630 0707-830) 5—11 (200-)437(-650) (950—)2123(—1500) + —
(350-)534(-800) (430—)628(-920) (700 0040-11500 5-7 (300-)527(-900) (1200—)2475(-5500) + —
(330 0608-850) (580—)662(-760) (760—)057(-1170) 5 (350—)850(-1450) (1800 2775-0300) + +
ue : 150-)891(-960) (1000—)1177 3—4 (450-)929(-1500) (1300-)2777(-4500) + —
(-1000) (-1350)
(57 are 30030) (7003851 (930—)1 109 3-12 (5001000 (900-)3600(-6700) + +
(-1160) (-1270) (-1450)

(2100530 C650) (570-)628(-700) (600-)783(920) 4-6 (550-)830(-1150) (1100-)2510(-2900) ~ —
(370—)636(-870) (750-)790(-850) (930—)1041 1-6 650-633 (1300—-)2511(-5200) + +
(1170) (1800)

(160—)393(-520) (420 )45 50470) (450-0523600) 3—4 (250-4211050) (550-)924(-1555) = =
(490—)649(-840) (540-)590(-700) (670-)835(-1070) 5-8 (450-J658(-900) (950-)2046(-3200) = —
(210-)296(-390) (300-)318(-350) (390-)450(-520) 3-1 (250-)383(-750) (350-)700-12000 = —
(450-)642(-850) |(560—)764(—880) (1100-01324 5-6 (300—)556(-900) | (500—)1397(—2400) s -

—1650)
(210-)381(-500) (420-)467(-550) (: DD ens 30) 4-6 (100—243(-400) (200 0) 301400) = —
(380-)696(-950) (620—)824(-950) (920-1 I: 3-5 (200—-)323(—450) (450-)1458(-2050) + =

E

574 Annals of the

Missouri Botanical Garden

Table 1. Continued.

Vessels
Helical
Percent- thicken- Helical
Secretory age of alari- Alte ing thicken-
ducts in scalari- Opposite ре nate ind дека ings Tangential
pith or form sel- vessel- vessel- sel- put in fibers diameter of
primary perfora- Number ay ray ray ay vessel and/or vesse : M a Vessels per
Species studied xvlem tions of bars Sind pitting pitting йык elements. tracheids square mm
V. barandan-
um var. bar-
andanum ? 20 (1213325) + + — + — — (30—)40(—50) (31 053065)
V. berberidifol-
ium = 90 (9-)12(-14) + + + — + — (11A 16021) 240-2940210)
V. bracteatum ? 50 (6—)9(—13) + + — + + -= (20—)32(—50) (165-)210(-260)
V. calycinum ? 90 (1-)15(-33) + + — — — — (20-)25(—40) (190—)242(—360)
V. consangui- ? 25 (5313-15) + t + + + — (30—-)38(-45) (81—)107(—124)
neum
V. corymbod-
endron ? 80 (41—12(-18) + + + + — — с, 410) (76-)106(-126)
V. corymbosum — 80 (2-)9(-19) + + E — + — 16022) (380—)430(—495)
V. cumingian-
um ? 5 (1-)3(—5) + + — + — — (15-)80(-45) (72 079-888)
V. exaristatum ? 5 23815) + + — + — — (30338(250) (52-)73(-102)
V. exul ? 80 (8-)8(-12) + — + — — = (23-)42(-60) (42-)61(—83)
V. floccosum ? 30 (3-)6(29) + + — — — — (25-)37(—60) (82 01030140)
V. floribundum — 90 (1-)9(-18) + + + — + — (10 14020) (280-0 3340380)
V. globulare ? 0 0 sh — + - + + (15—)19(—30) (160-)297(-360)
V. leschenaultii ? 40 (2—)9(—14) + + + — — — (25-)34(-40) | (66—)83(—100)
V. leucanthum ? 60 (137210) + + + — + — (153310) (92—)107(—128)
V. maderense ? 75 (1-)3(-6) ius + — — + — (1525-35) (470 0210240)
V. membrana-
ceum ? 85 (6-)11(-16) + + — — + = (15—)21(—30) (220-)273(-300)
V. meridionale ? 0 0 + — + — — — : (20-)23(-26)
(—105)
V. myrtillus — 90 (510-14) + + — — — = (15-)18(-25) (285—)344(-400)
V. occidentale ? 60 (4—-)8(-11) + — + — — — (131825) (290-4030448)
V. ovatum ? 100 (8—12(-15) + + — + + + (15-)22(-30) (200—)238(-289)
V. parvifolium ? 100 (6-)9(-12) + + — — + — (15-)17(-20) (210-2630300)
V. puberulum ? 90 (2-)6(-11) sk + — + — — (25-)32(-40) (80 0100120)
var. sub-
crenulatum
V. scoparium ? o0 (2-)4(—8) + + — = - — (12-)16(-25) (310-3360390)
V. stanleyi 70 (2-)7(-10) + + — un — — (45021030) (250-280-310)
V. uliginosum — 15 (1-)4(-6) + — + Е — — (10) 14(-20) (360 04210480)

Volume 91, Number 4 Lens et al. 575
2004 Wood Anatomy of Vaccinieae
Table 1. Extended. Continued.
Rays
Crystals
Multi- :
Vessels Tracheids Fibers se iate Present
v width in axial
Length of vessel Length of tracheids Length of fiber (number Height of uniseriate Height of multiseriate Present paren-
elements (um) (um) tracheids (um) И cells) rays (um) rays (jum) in rays chyma
(470-)695(-960) | (430—)663(—830) (860—)999(-1120) 1-7 (200-)400(-650) |(500—)1217(—-1800) = =
(370—)517(-650) | (430—)507(—510) (510-0018810) 2—5 (100-)583(-800) | (700-)986(-1600) = =
(300—487(-600) | (170—)087(-970) | (900—)1081 5-6 (350—)563(-1100) (700-)1408(-3000) — >
(1300)
(270—422(—520) |(390—)508(—000) | (450-)598(-700) 3-4 (150—-)286(—150) | (300—)61 7(—1100)
(520—)721(-920) (700—)776(-850) (640-0102 I-5 (250-)554(-1200) (400—)1059(—1 600) - -
(1210)
(450 00108850) (440-650-8300) (750-005 T1000 5— (250-)14.1(-600) (8000 01079-1500) — ت‎
(200—)298(—100) | (310—)368(—520) | (350-)526(-050) 3 (200-)486(-1150( (500—)1389(—1200) + -
(410-)596(-830) | (500—)644(—750) | (840-)930(-1 160) 5 (100—)586(—900) | (800—)1 823 (23300) + >
(360—)539(-690) | (430—)678(—830) (680—)943(-1170) 1-7. (2504631050) (400—) 1055(—2 100) = -
(570910 (890-3942 O 108 6-12 (350-)750(-1100) (800-)1725(-3700) — —
—1170) (-1050 910)
(370-)907(-830) | (530—)640(—720) e 0-) Е 3-0 (150-)886(-1700) (900—)2001(—6800) = =
(-113
(360—)389(—880) (290—)423(—190) (440—)5 pm 5-7 (150-)275(—450) A 500-)728(-850) = =
(26033872570) (3003832520) (330—)435(—520) 7 f = =
(520-)737(—930) (750—)942 (1020—)1 E I-6 (300-)585(-1050) — (10(-2500) + =
(-1020) (1450
(320-)536(-880) |.(450—)506(—600) (830-) "н 3 3-6 (350-)522(-700) (500—)868(—1200) =
(-12
(250—)448(—570) (400—)545(—510) o —140) 9 (200-0275 400) |. (450—)933(— 1300) = =
(230—)366(—170) 1 —280) ᷣ (370 04930580) 3 (300—)479(—750) | (500—)643(—1050) — =
(430—)739 (000 E a (1320-)1510 1-5 | (350-)581(-1050) (750—)1844(—3900) + =
(-1040) c (-1800)
DN ip pera (22 E 350) (870—)564(—680) 4-5 (200- ie Bape (350—)725(-950) = =
(150-)220(-320) (1: > -)210(-250) (220—)302(—380) 3—4 (150—)263(—350) | (350-)685(-1150) = =
(3305 en em (270-)394(-520) (630—)771(-950) 4—5 (500- soni E (650—)912(—1500) + =
(300-)403(—510) (270—)414(-560) (450-504(-710) 2-3 (30033 00) (350-)538(-950) + de
(570—)697(—800) | (350-)450(-600) - (890—) 104.2 —5 (450-)7 mi 0 ) (11002)1930(-2700) + =
(1340)
(170-)256(400) (200-(251) (280330370) — 3 — (150-)207(-300) (250-)475(-050) BA. =
- 280)
(230—438(-600) (180-0522-620) (680)-)783 15 (250-)367(-650) (500-)1045(-1700) = -
(-1030)
(130-)242(-350) (270—)341(—410) | (370—)400(—450) 1-5 (200-)275(400) (400-)575 1050) e ES

Annals of the
Missouri Botanical Garden

be rather arbitrary to distinguish intermediate cell
types to one of these categories, because their def-
1980:
Carlquist, 2001). Therefore, we prefer to give a de-

inition remains a matter of dispute (Baas,

tailed description of these cells. We consider tra-
cheids to be long and narrow cells, with dense pit-
ting in tangential walls (more than 15 pits per 100
um of tracheid length) and radial walls (more than
20 pits per 100 jum of tracheid length). These pits
are distinctly bordered and form two or three lon-
gitudinal rows in the radial and tangential walls
(see Fig. 3H). Fiber-tracheids represent the most
common cell type of the ground tissue. They are
somewhat longer than tracheids, narrow, thin- or
thick-walled, and contain one single row of dis-
tinctly bordered pits in tangential walls (ca. 5 to 15
pits per 100 рт of fiber-tracheid length) and radial
walls (ca. 5 to 20 pits per 100 рт of fiber-tracheid
length). The mean distance between two fiber-tra-
cheid pits in the tangential wall is longer than the
distance between two tracheid pits, although the pit
borders do not differ in size (ca. 3-6 um). Libriform
fibers are generally as long as fiber-tracheids. They
are narrow, mostly thin-walled and septate, and
show few to very few, minutely bordered to simple
pits in the tangential walls. The pit borders in the
libriform fibers are 2-3 um in size, and their den-
100 um of
length in tangential walls, and from 2 to about 10
per 100 рт of length in radial walls. Sometimes
only two or three pits are observed near the end of

sity ranges from less than 1 to 4 per

libriform fibers. Septate fiber-tracheids and inter-
mediate cells between septate libriform fibers and
fiber-tracheids are also seen in most species. For
all measurements of tracheary elements, only clear-
ly identifiable cells were taken into account.
Wood features were plotted on trees using the
program MacClade 4.04 (Maddison & Maddison,

200:

RESULTS

Woods of most species have indistinct growth
rings and are diffuse-porous (Figs. 1, 2), although
a few species of Cavendishia, Satyria Klotzsch, Thi-
baudia J. St.-Hil., and Vaccinium (Fig. 1C) show a
tendency to semi-ring-porous wood. Vessels are an-
gular and mainly solitary. (Figs. 2). although
some tangential vessel groupings of 2 to 4 cells are
reported in several genera. The mean tangential
vessel diameter ranges from 14 jum in Vaccinium
uliginosum to 164 jum in Dimorphanthera kempter-
tana with an overall average of 35 um. Likewise.
the two species mentioned show extreme mean ves-
sel density values (421 and 12 vessels per square

mm, respectively), while the mean value for the en-
lire tribe is 145 vessels per square mm. The mean
length of the vessel elements is 600 wm and varies
from 220 jum in Vaccinium occidentale to 1006 wm
in Disterigma cryptocal yx.

Vaccinieae often have mixed simple and scalar-
iform perforation plates, although the scalariform
type usually dominates. Genera with species having
mostly scalariform perforations include Anthopterus
Hook., Ceratostema Juss., Demosthenesia A. C. Sm.,
Diogenesia Sleumer, Disterigma (Klotzsch) Nied.,
Lateropora А. C. Sm., Gaylussacia, Mycerinus A. C.
Sm., Plutarchia A. C. Sm., Oreanthes Benth. (Fig.
3D), Orthaea Klotzsch (Fig.
Klotzsch, Symphysia С.

ЗС). Semiramisia
Presl, and Sphyrospermum
Poepp. & Endl., while simple perforations dominate
Notopora Hook. f.,

Polyclita A. C. Sm., and Siphonandra Klotzsch; the

in Dimorphanthera Y. Muell.,

other genera show more variation in the type of
vessel perforation between the species observed, for
К) and Vaccinium
(Figs. 3B, К). Intervessel pits are scarce and mostly
opposite (2-5

example, Agapetes (Figs. 3A,

5 jum in size) to scalariform (6-20 um
in size), except in Agapetes and Vaccinium, which
often show alternate intervessel pitting (2-5 um in

—

size). Vessel-ray pits are scalariform with strongly

4E-H) ex-

cept for Agapetes, Gaylussacia, and most Vaccinium

reduced borders in most genera (Figs.

species, and range from rather small (6 jum in size

—

to very large (40 um in size in species with wide
vessels). Alternate vessel-ray pits with distinct bor-
ders are typical of Agapetes (2-5 jum in size, Fig.
4D).

ting is observed.

while in Vaccinium all types of vessel-ray pit-

Helical thickenings are nearly always present in
the tails of vessel elements; their presence through-
out the body of vessel elements is restricted to spe-
cies of Agapetes, Disterigma, Ceratostema, Gaylus-
sacia, and is especially common in Vaccinium (Fig.
3G).
some fibers and/or tracheids of Agapetes, Disterig-
ma,

Helical thickenings were also observed in
and Vaccinium.

The ground tissue of the wood consists of fiber-
tracheids, except for Dimorphanthera collinsii, D.
cornuta, and Macleania rupestris, in which tra-
cheids form the ground tissue. The fiber-tracheids
have very thin to thick walls. The mean length of
the fiber-tracheids is 865 pm with a minimum
Vaccinium occidentale
and a maximum mean length of 1516 um in Vac-

mean value of 302 um

cinium meridionale. Occasionally thin-walled libri-
form fibers, which are usually septate with few sim-
ple to indistinctly bordered pits, were reported in
all species, except for Dimorphanthera kempteri-
ana, Macleania crassa, M. rupestris, Satyria sp. in-

Lens et al.

Volume 91, Number 4
2004 Wood Anatomy of Vaccinieae

еа,"
PAS AE
@ VENE
(7 52
va HER

q 2,*
AR

LI 13
N
FORE T

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ue
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. 2. a
Of I aoe
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Figure l. A-H. Transverse sections showing arrangement of vessels, distribu
—A. Agapetes flava (Grierson & Long 3076. E 198224
| ] 1 calycinum (Stern 2950, Tw 24121). —D. Vaccinium puberulum var.
— Е. Notopora schomburgkii (Maas et al. 5808, Uw 27397). —F. /

,. Lateropora ovata (Luteyn 15294, NY). —H. Diogenesia

thickness of fiber walls.

pubiflora (Vink 17307, Kw 11639).
subcrenulatum (Maas et al. 5733

misia cf. ulbrichiana (Luteyn &
tetrandra (Luteyn et al. 7388, N

Aes

көө. >

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52 iia
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brén-Luteyn 6532, NY

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tion of axi
3). —I

578 Annals of the
Missouri Botanical Garden

MN ¡YA e M
(eu * 1215 22 Ad
994 ч a’ 0.0 O's,"
- 39:9 è 12 N .
que АГ 52 v
N: a C DA D
E 218 Ne 7

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Figure 2. A-F. Transverse sections showing arrangement of vessels, distribution of axial parenchyma (arrows), and
thickness of fiber walls. —A. Sphyrospermum sp. indet. (Argent, E 19762390). —B. Demosthenesia spectabilis (Luteyn
6452, NY). —C. Cavendishia bracteata (Dorr et al. 6890, Lw). = Macleania stricta (Luteyn & Lebrón-Luteyn 57 744,
NY). —E. Orthaea fimbriata (Luteyn & Lebrón-Luteyn 5794, NY). —F. Satyria meiantha (Breedlove 9746, MADw
23933)

det. (Uw 17005), Siphonandra elliptica, Themisto- (Fig. 3H), although they were not observed in Dis-
clesia pendula, T. vegasana, and Vaccinium — terigma cryptocalyx, Vaccinium membranaceum, V.
meridionale. The libriform fibers are somewhat myrtillus, V. occidentale, and V. puberulum. In Di-

shorter than fiber-tracheids (on average 700 jum) morphanthera collinsii and D. cornuta, the ground
and contain nuclei (Fig. 5H). Also septate fiber- tissue is formed by tracheids only, which show

tracheids and cells intermediate between septate large, bordered pits usually between 6 and 9 jum
libriform fibers and fiber-tracheids were observed in size.
in most species. In general, tracheids are present The main distribution type of the axial paren-

Volume 91, Number 4 Lens et al. 579
2004 Wood Anatomy of Vaccinieae

Figure 3. XC. Se ‘alariform vessel perforations. А. . 1 в (Burtt 958, Е 19672592). —B. Vaccinium
angustifolium (Lens, BR). —C. Orthaea fimbriata (Luteyn & Lebrón-Luteyn 5794, NY). —D. Vessel perforation mixed
scalariform and m Drésnihas ecuadorensis (Luteyn 15394, NY ). EF Simple vessel pe carre E. Agapetes
sikkimensis (Sinclair & Long 5778, E 198421 — К. Vaccinium globulare 7 8 ни 1460, Tw 46335). —G. Helical
thickenings throughout vessel element: у, ovatum M a. 1418, 'Tw 46267). —H. Trache е Dimorphanth-
era kempteriana (Vink 16888, Tw 23733)

580 Annals of the
Missouri Botanical Garden

ү
ШИ)

| | | ии ШҮ ү

4
25075 E
== М

*
ка *
r

— Ó—À }
16 um

Figure 4. A-C. Radial sections showing structure of multiseriate rays. —A. Proc nm ‘nt, square and m body

ray cells: Agapetes mannii (Kingdon-Ward 19097, E 19500046). —B. Exc lusive ly procumbent body ray cells: Vaccinium
ү (Wiemann 13, Uw 30897). —С. Mainly upright and . are body ray cells: Macleania pe а (Luteyn
c Lebrón-Luteyn 6957, NY). D-H. Vessel-ray pitting. —D. Vessel-ray pits bordered: A Igapetes sikkimensis (Sinclair &

78, E 19842032). E-H. Vessel-ray pitting scalariform with i reduced borders. —E. 5 kemp-
teriana (Vink 16888, Tw 23733). —F. Orthaea fimbriata (Luteyn & Lebrón-Luteyn 5794, NY). —G. Macleania loese-
neriana (Luteyn & Lebrón-Luteyn 5726, NY). —H. Oreanthes ecuadorensis (Luteyn 15394, NY).

Volume 91, Number 4 Lens et al. 581
2004 Wood Anatomy of Vaccinieae

FFE

р eee
TP Eri
—
ELT e —
A —— —

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M AN
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10 |

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HOG са "e|
х А
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2 „
Lev. e.
IA Fa

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е.

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Los:
272

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т

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7023,

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T СУ а H
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SA Е
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een 2
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eee

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Figure 5. Tangential sections showing the width of multiseriate ravs А. Agapetes flava (Grierson & Long 3076.
D D А e d é

D me ww n
E 19822403). —B. Vaccinium barandanum var. barandanum (Jacobs 7249, Uw 33743). —C. Vaccinium floribundum
(De Sloover 399, BR). —D. Vaccinium uliginosum (Dechamps 6033, Tw 38581). —E. Satyria sp. indet. (Maguire et al.

48650, Uw 16976). —E. Polvclita turbinata (Luteyn 15453, NY). —G. Psammisia cf. ulbrichiana (Luteyn & Lebrón-
Luteyn 6532, NY). —H. Nucleus (arrow) in septate libriform fiber: Gaylussacia baccata (F. Lens. BR).

582

Annals of the
Missouri Botanical Garden

chyma is scanty paratracheal (Figs. 1, 2); sparsely
diffuse apotracheal parenchyma was also seen in
species of Agapetes, Cavendishia, Ceratostema, Di-
morphanthera, Orthaea, Psammisia, Satyria, Thi-
baudia, and Vaccinium, while diffuse-in-aggregates
parenchyma was observed in some Vaccinium spe-
cies. Banded marginal parenchyma was seen in a
few species, viz. Agapetes flava (Fig. ТА), Mycerinus
chimantensis, Notopora schomburgkii, Psammista
cf. ulbrichiana (Fig. IF), Satyria sp. indet. (Luteyn
& Lebrón-Luteyn 7177, NY), and Sphyrospermum
sp. indet. Axial parenchyma strands usually consist
of 2 to 4 cells, although strands with up to 8 cells
were also observed. In almost all genera, except for
Gaylussaccia and most species of Vaccinium, un-
divided (fusiform) axial parenchyma cells were
seen, ranging from 350 pm to 1050 um with an
average length of 600 um. Intermediate types be-
tween fusiform axial parenchyma cells and libri-
form fibers also occur.

Uniseriate rays consist of predominantly upright
cells. The mean height of the uniseriate rays varies
greatly from 207 jum in Vaccinium uliginosum to
2478 um in Psammisia graebneriana, with an ау-
erage height of 740 um for all species studied.
Chambered cell types and prismatic crystals are
always absent within uniseriate rays.

Multiseriate rays are heterocellular and usually
consist of procumbent, square and/or upright body
ray cells and several rows of upright marginal ray
cells. In Agapetes, Dimorphanthera, Disterigma,
Gaylussacia, and Vaccinium, however, upright body
ray cells are rare while procumbent and/or square
body ray cells dominate (Figs. 4A, B). Multiseriate
rays are in general 3 to 7 cells wide (Fig. 5). Narrow
rays (2- to 3-seriate) were observed in juvenile
stems of Cavendishia compacta, Macleania ericae,
and Mycerinus chimantensis, while wide multiser-
iate rays (sometimes more than 10 cells wide) were
seen in several Agapetes species (Fig. 5A) and in
Dimorphanthera dekockii, Disterigma alaternoides,
Satyria panurensis, Themistoclesia epiphytica, Thi-
baudia floribunda, Thibaudia pachypoda, and Vac-
cinium exul. Multiseriate rays are much higher than
uniseriate rays, mostly between 1000 and 7500
pm, with an average height of 4020 pm. Multi-
seriale rays in some species are without doubt
much higher than indicated by the measurements
in Table 1, since the height of the multiseriate rays
often exceeds the length on the section. Very high
rays (more than 10,000 jum) were observed in spe-
cies of Agapetes, Disterigma, Macleania, Psammi-
Sheath
cells are mostly present, but not always clearly de-

sia, Satyria, and Themistoclesia Klotzsch.

veloped. Gummy deposits (possibly tannins) were

frequently noticed in the ray cells (Figs. 4B, C,

л

Prismatic crystals occur in non-chambered гау
cells (Fig. 6A) or in chambered ray cells (Figs. 6B,
С), but they were absent in species investigated of
Demosthenesia, Diogenesia, Gaylus-
sacia, Oreanthes, Plutarchia, Semiramisia, Siphon-
andra, and Symphysia. Sometimes they are ob-

Ceratostema,

served in chambered axial parenchyma cells of
Anthopterus, Cavendishia, Disterigma, Macleania
(Fig. 6E), Psammisia (Fig. 6D), Themistoclesia, and
Thibaudia.

The pith structure of the Vaccinieae species in-
vestigated is homogeneous. In Demosthenesia, Gay-
lussacia, Oreanthes, Plutarchia, and Symphysia no
crystals were observed in the pith, but the remain-
ing genera show prismatic crystals and/or druses.
In Notopora cardonae and Polyclita turbinata (Fig.
61), thick-walled sclereids are observed among the
pith cells. Secretory ducts at the border of the pri-
mary xylem and the pith, but sometimes also in the
pith, were observed in species of Cavendishia, De-
mosthenesia, Diogenesia, Lateropora, Macleania,
Oreanthes (Fig. 6H), Orthaea (Fig. 6F, C). Polyclita,
Semiramisia, Themistoclesia,

Psammisia, Satyria,

and Thibaudia.

DISCUSSION

Our wood anatomical observations largely agree
with the earlier description of Vaccinieae by Met-
calfe and Chalk (1950), although some differences
can be found. For instance, the width of the vessels
is generally reported to be between 25 and 50 jum
and only slightly larger in Paphia. We have ob-
served several species with a mean tangential ves-
sel diameter of more than 80 jum. Furthermore,
Metcalfe and Chalk (1950) mentioned that helical
thickenings throughout vessel elements are restrict-
ed to Vaccinium, but this study has shown that
these thickenings are also present in species of
Agapetes, Ceratostema, Disterigma, and Gaylussa-
cia. In addition, helical thickenings are found
throughout fiber-tracheids and/or tracheids in Aga-
petes mannii, Disterigma sp. indet., Vaccinium ar-
boreum, V. globulare, and V. ovatum.
mentioned authors also underestimated the height
of the multiseriate rays (commonly more than 1000
um), but Giebel (1983) found a more correct value
for the height of multiseriate rays in Cavendishia,
3 and 7021 jum.

striking new character is the observation of secre-

The above-

i.e., often between 107: The most
tory ducts in the primary xylem and pith of 13 gen-
era belonging to the Andean clade, which has not
been recorded previously as far as we know. The

Volume 91, Number 4 Lens et al.
4 Wood Anatomy of Vaccinieae

Figure 6. A-C. P W көнө in гау ce "m —A. 8 -€ qu ray cells: Dimorphanihera е (Vink
16888, Tw 23733). В, Chambar ray cells pe Mycerinus chimantensis (O. Huber 9010, NY otopora
schomburgkii (Maas et a 808, Uw 27397). D. E . Prismatic crystals in chambered axial paren а cells. —D.

—E. Macleania crassa (Luteyn et al. 7378, NY). F-H.

‘eines sp. indet. (van x n et al. 359, da 25565).
». Transverse section (arrows): Orthaea fimbriata (Luteyn & Lebrón-

'retory ducts in primary xylem and pith. —
E. 5794, NY). —H. v таш section e secretor rrows) around a secretory duct (SD): Oreanthes
ecuadorensis (Luteyn 15394, NY). —1. Sclereids in pith: Polyclita Eod (Luteyn 15453,

584 Annals of the
Missouri Botanical Garden

il Vaccinium membranaceum
ium
Bl Vaccinium ae Myrtillus clade

mV oy inium parvifolium
i
==: ussaci a baccata

ah oa ‘hosseana | | Agapetes clade

Vaccinium consangunsam
¿53 Vaccinium floribundum
EN gi Dimorphanthera pns cki
ii Dimorphanthera Esas
ШЕ Notopora schomburgki

East Malesian clade

gw Disterigma alaternoides Andean clade
y

—

ШЕ Thibaudia pachypoda

ШЕ Siphonan ra ell tica
ra

а Macleania hi
| f gi Macleani Пп
ШЕ Macleania
1 ШЕ Ceratostema | reginaldi

Psammisia ulbrichiana
lg Psammisia ecuadorensis
ll Symphysia racemosa | Meso-American/Caribbean clade

arrangement of vessel-ray pitting
unordered
opposite to alternate
opposite to scalariform
BN exclusively scalariform
variable
[ITI] equivocal
Figure Modified tree based on the mole c ular а 's of Kron et al. (20020) and Powell and Kron (2002, 2003)
showing the arrangement of vessel-ray pits in Vaccinieae. Clades one, two, and three represent an intermediate group
based on their wood structure. Arrows cae iicet 1 s of at least 85%.

~

exact contents of these secretory ducts is unknown. Gaylussacia baccata and Vaccinium angustifolium.
When unbleached, longitudinal sections were ob- Besides these two species. it is known that other

served, a brown substance was sometimes seen, but Vaccinieae species contain living fibers, namely
the secretory duct also seems to be empty in many Vaccinium myrtillus, V. varingiaefolium, and spe-
cases (Fig. 6H). It is also unclear whether these cies of Cavendishia (Wolkinger, 1970; Giebel,

secretory ducts are present in other vegetative tis- 1983). It is generally accepted that nuclei in sep-
sues tate fibers persist much longer than in fiber-tra-

8.
We also found nuclei in septate libriform fibers cheids and tracheids. Nuclei in septate fibers are
of the two species that were stored in FAA, namely likely to be found in Vaccinieae, if fresh material

Volume 91, Number 4
2004

Lens et al.
Wood Anatomy of Vaccinieae

585

О Vaccinium meridionale
El Vaccinium ovatum

L] Vaccinium floribun

pongas epiphyt

Ш Symphysia racemosa

type of vessel-ray pitting
unordered

С] distinctly bordered
ШЕ] minutely bordered
EN nearly) simple
[TIT] equivocal

—

Figure 8. Modified tree based on the molecular analyses of Kron et al.

Vaccinium раги ойи oliu m

Demosthene Fa

1 dater noides
E Sphyros um buxifolium

[] Vaccinium membranaceum

Myrtillus clade

| Agapetes clade

El Vaccinium corymbodendron

accinium c y rad eel

East Malesian clade

Andean clade

| Meso-American/Caribbean clade

(2002b) and Powell and Kron (2002, 2003)

3 the type of vessel-ray pits in Vaccinieae. Clades one, two, and three represent an intermediate group based
on shale wood structure. Arrows indicate bootstrap values of at least 85%.

is preserved in FAA. Since Vaccinieae and the
subfamily Vaccinioideae as a whole is character-
ized by septate fibers, it is expected that nucleate
fibers are typical of the subfamily. Indeed, several
authors have noticed the presence of living fibers
in Vaccinieae (Braun, 1961; Fahn & Leshem,
1962; Giebel, 1983) and other tribes of the sub-
family (Lens et al., 2004a). However, there are
also records in Arbutoideae, another subfamily of

Ericaceae, in which septate fibers

(Wolkinger, 1970).

PHYLOGENETIC WOOD ANATOMY

are found

In order to comment on the recent generic re-

alignments within the tribe and to trace the evo-

lution of some important wood anatomical charac-

ters, we have created a tree, based on the molecular

phylogenetic studies of Kron et al.

(2002b) and

Annals of the

Missouri Botanical Garden

OSS

um angustifolium
nium corymbosum
nium arboreum

niu m co
nium тане
nium ovatum
inium consan
1 floribundum

acc
acc
с

———ů— 2

H

a
wm Orthaea fi fim ria a
a Cayenne pres teat
E Thibaudia ТШ.
Satyria BAUL fale
Bi Ѕаїугіа warszewiczil
msatyria m
D Disterigma 'alater noides

Bl Psammisia ecuadorensis
m Symphysia racemosa

shape of body ray cells in multiseriate rays
unordere
main procumbent

MA procumbent, square and upright
BN square and upright

ШТП equivocal

Figure 9. Modified tree based on the molecular analyses

showing the shape of body ray cells in multiseriate rays of Vaccinieae.

intermediate group based on their wood structure. Arrows ine

Powell and Kron (2002, 2003). The tree contains
45 species and 20 genera that are included in this
study and represents all major evolutionary lines in
Vaccinieae, the Bracteata-Oarianthe
This clade, comprised of species of Vaccin-

except for
clade.
ium from New Guinea and Borneo,
from this study due to lack of material. As indicated
by arrows, the subclades with an informal name
have bootstrap values of at least 85%, but relation-

was omitted

ships between these clades are poorly supported

(Figs. 7-10). Therefore, our discussion of the re-

Bl Dimorphanthera dekockii
imorphanthera рои
urgki

um buxifolium

lium membranaceum

Myrtillus clade

| Agapetes clade

rymbodendron

guineum

East Malesian clade

Andean clade

Meso- American / Caribbean clade

of Kron et al. (2002) and Powell and Kron (2002, 2003)
and th represent an
licate bootstrap values of at least 85%.

Clades one, two, ree

lationships within Vaccinieae is focused on the
named subclades.

‘our wood characters are plotted on the tree,
i.e., arrangement of vessel-ray pitting (Fig. 7), the
type of vessel-ray pitting (Fig. 8), the shape of
body ray cells in multiseriate rays (Fig. 9), and
the presence of secretory ducts (Fig. 10). These
features are chosen based on their apparent con-
sistency within the various subclades of Vacci-
nieae and on previous studies within the family

2003, 2004a).

(Lens et al.,

Lens et al.

Volume 91, Number 4
2004 Wood Anatomy of Vaccinieae

Myrtillus clade

O Gaylussacia p

Vacc
ARE м
П Vaccinium en
O Vaccinium corymbosum
accinium arboreum
accinium corymbodendron
accinium meridionale

| Agapetes clade

D
О
оо
2.2
Ec
29
S

consanguineum
нт floribundum
imorphanthera deko

Ckii "
imorphanthera kempteriana East Malesian clade
rakii

O
AFZ OO
> 8
O O
O =
Q
y
o

mH m OO m "RENNES
— f f f 23 »

d epiphytica
De ا الا‎ A
Orthaea finn

Cavendishia bracteata
hibaudia jahni

|

Andean clade

Jftimrmrm
a
ct
< Ф
23237.
@®®
=
Ф
m
tb
ct

o
D
$60

m

t5

udia martiniana
a pa chypoda
ra elli

=.

—»
<=
m

zo
o
6]
£D
=,
t5
2.

Meso- American / Caribbean clade

JO Symphysia racemosa

presence of secretory ducts
unordered
absent
ШШ present
Modified tree based on the molecular analyses of Kron et al. (2002b) and Powell and Kron (2002, 2003)
in the primary xyle m and the pith of Vaccinieae. Clade two, and three
| on their wood structure. Arrows indicate bootstrap values of at least 85%.
le.

Figure 10.
donne the. presence of secretory
represent an intermediate group. base
Missing blocks indicate that the pith and primary xylem tissue was not availa

б ducts es one,

narrow (2- to 5-seriate) and low multiseriate rays
(often lower than 1000 um) with mainly procum-
"ig. 9). It is remarkable that

Myrtillus Clade (represented by Vaccinium

calycinum, V. membranaceum, V. myrtillus, V.

arvifolium, V. bent body ray cells (Fig.
Ó ) 8
this set of characters is common in non-vaccinioid

1948; Suzuki & Noshiro.

scoparium, and V. sp. indet.
Hawaii)
Ericaceae (see also Cox,
The enlarged Myrtillus clade sensu Powell and 1988) |
Kron (2002) mostly occurs along the Pacific Rim
T

from Japan to Mexico (Powell & Kron, 2002). The

species studied are wood anatomically defined by
the presence of exclusively or mainly scalariform
perforations, opposite to scalariform vessel-ray pit-
ting with distinctly bordered pits (Figs. 7. 8). and

Agapetes Clade (represented by Agapetes hosseana
only)

This clade contains temperate and tropical Asian
Vaccinium species and species of Agapetes (Kron et

588

Annals of the
Missouri Botanical Garden

al., 2002b). Although we have studied several Aga-
petes species, only A. hosseana is included in the
molecular tree. This species shows some features
that resemble the Myrtillus clade, for instance, the
presence of distinctly bordered vessel-ray pitting
(Fig. 8), and the relatively narrow and low multi-
seriate rays. On the other hand, other Agapetes spe-
cies investigated are characterized by very broad
(3- to 15-seriate) and high multiseriate rays (some-
10,000 um in A
A. moorei). The only characters that seem to distin-

times more than . sikkimensis and
guish this group from the Myrtillus clade are (1)
the presence of alternate vessel-ray pitting, which
is also seen outside the Agapetes clade in a few
Vaccinium species and in many non-vaccinioid Er-
icaceae, and (2) the occurrence of procumbent,
square and upright body ray cells in the multiser-
iate rays, although this type of ray composition is
also seen in Vaccinium membranaceum (Figs. 7, 9).

East Malesian Clade (represented by
Dimorphanthera dekockii and D. kempteriana)

The East Malesian clade comprises species be-
longing to Dimorphanthera and Paphia (Kron et al.,
2002b). The two Dimorphanthera species that are
used in this study differ from the Agapetes and
Myrtillus clades by the presence of wide vessel el-
ements (ranging from 60 jum to 205 qum) with al-
most exclusively simple perforation plates, mainly
scalariform vessel-ray pits with strongly reduced
borders (Figs. 7, 8), and the occurrence of prismatic
crystals in multiseriate rays. Furthermore, the two
species studied are also defined by an abundant
presence of tracheids and a small amount of fiber-
tracheids, and broad (4- to ll-seriate) and high
multiseriate rays (1800-8400 um).

centage of wide

The high per-
vessels with simple perforations
and the abundant occurrence of tracheids is likely
due to the climbing habit of Dimorphanthera (see
also Lens et al., 2004b).
Meso-American/Caribbean Clade (represented by
Symphysia racemosa only)

This is a well-supported clade that contains spe-
cies generally found in Central America and the
Caribbean (Kron et al., 2002b).
amined in this study shows mainly scalariform ves-

ШЫ .
The species ex-

sel perforations, exclusively scalariform vessel-ray
pits with strongly reduced borders, and relatively
narrow multiseriate rays (4-seriate) with procum-
bent, square and upright body ray cells (Figs. 7—
9). It is worth mentioning that similar vessel-ray
pits are found in the East Malesian clade and the
Andean clade.

Andean Clade (represented by Anthopterus маган,
Cavendishia bracteata, Ceratostema reginaldii,
Demosthenesia spectabilis, Disterigma alaternoides,
Macleania ericae, M. hirtiflora, M. stricta, Orthaea
fimbriata, Polyclita turbinata, Psammisia
ecuadorensis, P. cf. ulbrichiana, Satyria meiantha, S
panurensis, S. warszewiczii, Siphonandra elliptica,
Sphyrospermum buxifolium, Themistoclesia
epiphytica, Thibaudia floribunda, T. jahnii, T.
parvifolia, T. pachypoda, and T. martiniana)

The Andean clade shows by far the highest spe-
cies diversity within Vaccinieae, and is concentrated
in the moist, montane forests of the northern Andes.
This group has evolved very recently, about 20 mil-

ion years ago when the Andes began to rise (Luteyn,
2002). This can also be illustrated by its homoge-
neous wood structure. Species of the Andean clade
are characterized by scalariform vessel-ray pits with
strongly reduced borders (Figs. 7. 8). and by broad
(4- to 14-seriate) and high (often more than 3000
um) multiseriate rays with a high percentage of

-
=

square and upright body ray cells (Fig. 9). Further-
more, prismatic crystals often occur in ray cells as
well as in axial parenchyma cells. The most distin-
guishing character, however, is the occurrence of se-
eretory ducts near the primary xylem and the pith
tissue. All specimens with secretory ducts are in-
cluded in the Andean clade (Table 1), but this char-
acter is sometimes lacking in, for instance, the two
unplaced species, ie, Disterigma alaternoides and
Sphyrospermum buxifolium (Fig. 10).

thin the Andean clade, wood anatomical sup-
port for the division into the two major subclades
is lacking. Nevertheless, the sister relationship of
the Andean clade with the Meso-American/Carib-
bean clade seems justified according to wood ana-
tomical data: both clades show mainly scalariform
vessel perforations, scalariform vessel-ray pits with
strongly reduced borders, and distinctly upright
body ray cells (Figs. 7—9).

Remaining Subclades (represented by Gaylussacia
baccata, Notopora schomburgkii, Vaccinium
angustifolium, V. arboreum, V. consanguineum, V.
corymbodendron, V. corymbosum, V. exul, V.
floribundum, V. meridionale, V. ovatum, and У.
uliginosum)

Because the monophyly and the taxonomic po-
sition of the remaining subclades is still debatable,
it is difficult to speculate on the wood anatomical
trends in these groups. Wood anatomically, it seems
that clades one to three, comprising several Vaccin-
ium species and Gaylussacia baccata (Figs. 7—10,
clades 1—3). form an intermediate group between

Volume 91, Number 4
2004

Lens et al.
Wood Anatomy of Vaccinieae

the Myrtillus clade and the group including the
East Malesian clade, the Meso-American/Caribbe-
an clade and the Andean clade. Wood features that
illustrate the intermediate position of clades one to
three include the presence of (1) minutely bordered
pits in Gaylussacia baccata, Vaccinium corymbod-
endron. V. consanguineum, and V. ovatum (Fig. 8).
(2) prismatic crystals in ray cells of V. corymbosum.
V. meridionale, and V. oratum, and (3) relatively
broad (6-12-seriate in V. exul) and high multiser-
iale rays in some species (up to 4200 um in V
corymbosum). The taxonomic position of Vaccinium
uliginosum, which is placed as sister to the Andean
clade and the Meso-American/Caribbean clade. is
not supported wood anatomically because none of
the above-mentioned intermediate characters are
present.

The taxonomic position of Notopora schomburgkii
as sister to the East Malesian clade is wood ana-
tomically supported by the occurrence of simple
vessel perforations, scalariform vessel-ray pits with
strongly reduced borders (Figs. 7. 8). and the oc-
currence of prismatic crystals in the rays. Further-
more. the same features are also present in some
representatives of the Andean clade, as in. for in-
stance, Satyria meiantha, S. panurensis, Thibaudia
floribunda, and J. pachypoda.

The possible relationship of Dimorphanthera and
Satyria as suggested by Stevens (1974) is wood an-
atomically disputable: the two genera share several
similar wood features, like scalariform vessel ray-
pits with much reduced borders, high multiseriate
rays and prismatic erystals in ray cells. but these
features are very common in the Andean clade. In
addition, the two genera show a high percentage of
simple vessel perforations in their wood, a feature
that is relatively rare in the Andean clade. but this
is probably due to the climbing habit of Dimor-
phanthera and Satyria.

STRUCTURE OF MULTISERIATE RAYS

The taxonomic value of multiseriate rays with
mainly square and upright body ray cells in Vac-
cinieae is somewhat unexpected in a family con-

—

aining many shrubs with relatively thin stems. It
is known that upright body ray cells are abundantly
present near the pith while more procumbent cell
shapes are found closer to the cambium. Indeed,
the mean stem diameter of the Vaccinium species
studied is larger than the stem diameter of the An-
dean clade species. This could explain the pres-
ence of exclusively procumbent body ray cells in
Vaccinium in regard to the mainly square to upright
body ray cells in the wood of the Andean clade

species. However, thick wood samples of the An-
dean clade (e.g... Ceratostema reginaldii, Satyria
meiantha, and S. panurensis) and the East Malesian
clade (Dimorphanthera kempteriana) also show
many upright and square body ray cells. Moreover.
only mature stems of species belonging to the An-
dean clade were collected during various field trips.
This indicates that the shape of body ray cells con-
tains a phylogenetic signal within Vaccinioideae. as
mentioned by Lens et al. (2004a).

WOOD ANATOMICAL
ERICACEAE S.L.

COMPARISON WITH OTHER

The wood structure of Vaccinieae shows many
similarities with that of Ericaceae s.l. Examples in-
clude the diffuse-porosity, narrow and solitary ves-
sels with an angular vessel outline, high vessel fre-
and/or simple vessel

quency, — scalariform

perforations, tracheids, distinctly bordered fiber
pits (fiber-tracheids), scarcely distributed axial pa-
renchyma, and the combination of uniseriate rays

The

group Corresponds especially to other tribes of the

with less common multiseriate rays. study

subfamily Vaccinioideae as well as to the related
epacrids (subfamily Styphelioideae). As mentioned
(2003, 2004a), the presence of wide

and high multiseriate rays, which are nearly absent

by Lens et al.

outside Styphelioideae and Vaccinioideae, may
support the relationship between both subfamilies.
In addition, the sporadic occurrence of libriform
fibers and the presence of erystal-bearing axial pa-
renchyma cells are found in both subfamilies. but
these two features also occur in the distantly related
subfamily Arbutoideae (Lens, pers. obs.).

Most genera of Vaccinieae, except for the large
genus Vaccinium, can easily be distinguished from
other Ericaceae by a set of wood anatomical fea-
tures. These features include the presence of sca-
lariform vessel-ray pits with strongly reduced bor-
ders. high multiseriate rays (often more than 3000
pm) with mainly square to upright body ray cells
containing prismatic crystals, and the occurrence
of undivided axial parenchyma cells; which usually
range from 500 to 900 um.

CONCLUSIONS

The wood structure of the tribe Vaccinieae, con-
sidered to be a derived tribe within the Ericaceae.
fits well within the family and shows some taxo-
Many f

Vaccinium show several wood features that corre-

nomically important. characters. species «

spond with a typical Ericaceae wood sample: dis-
tinctly bordered vessel-ray pits. and narrow (2- to

d-seriate) and low (often less than 1000 um) mul-

590

Annals of the
Missouri Botanical Garden

tiseriate rays, which mainly consist of procumbent
body ray cells. Other clades within Vaccinieae, rep-
resented by the East Malesian clade, the Meso-
American/Caribbean clade, and the Andean clade,
show a set of characters that are absent in other
members of the family, viz. scalariform vessel-ray
pits with strongly reduced borders, a high portion
of upright body ray cells (although exclusively pro-
cumbent in Dimorphanthera kempteriana), wide (4-
to 14-seriate) and high multiseriate rays (often more
than 3000 рт). and prismatic crystals in cham-
bered ray cells (but absent in Symphysta racemosa).
Furthermore, the presence of secretory ducts in the
primary xylem and in the pith, which is frequently
observed in the Andean clade, seems to represent
a feature otherwise lacking in the family. In addi-
tion, the presence of long. non-divided axial paren-
chyma cells in most species of Vaccinieae distin-
guishes this tribe from the rest of the subfamily.

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Volume 91, Number 4 Lens et al. 591

2004 Wood Anatomy of Vaccinieae
characteristics for distinguishing aap myrtillus mm; D. kempteriana Schltr.: INDONESIA. East Iri-
from ESE vitis-idea. Preslia (Praha) 75: 85-91. an, Vink 16888 (Tw 23733), 44 mm.

Suzuki, M. . Noshiro. 1988. Pp. Er 351 in H. Ohba Diogenesia floribunda (А. C. Sm.) Sleumer: ECUADOR.
& S. В. AA (editors), Wood Structure in Himalayan »-Pastaza, J. L. Luteyn & M. Lebrón-Luteyn
Plants, Vol. 1. Univ. Tokyo Press, Токус 5675 (NY), 9 mm; D. tetrandra (A. C. Sm.) Sleumer:

Weingartner, D. P. 1969. Studies of Clee and Stem COLOMBIA. Cauca, J. L. Luteyn el oif 7388 (NY),
Blight Diseases of Highbush Blueberry (Vaccinium cor- 11 mm.

ymbosum L.) in Michigan. Ph.D. Thesis, Michigan State : PERU. Loreto, collector жү»
University, East Lansing. ( Н О), 10 mm; D. sp. indet.: PEI zaja-
Wolkinger, F. 1970. Das Vorkommen lebender CEP 'n marca, C. Carton 54 (BR), 8 mm: D. latent
in Sträuchern und Bäumen. Phyton (Austria) 14: Ned: "Col .OMBIA. Cauca, J. L. Luteyn et al. 7
67. NY), 11 mm: D. eryptocalyx А. C. Sm.: COLO И.
Huila , J. I. Luteyn & М. Lebrón-Luteyn 7545 (NY),
INDEX TO SPECIMENS EXAMINED T mm.
Gaylussacia baccata K. Koc Е 5 in FAA): ed
GIUM. F Lens (BR), 7 mm; С. decipiens Cham. var.
decipiens: BRAZIL. P. Pd 1840 (BR), 6 mm.

Disterigma sp. indet.
Tw 3138

The wood samples studied are listed below with refer-
ence to the origin, collec ‘lor, and the diameter of the wood
sample in mm. “Mature” means that the wood sample is Late pe ovata А. C. Sm.: M AMA.
derived from a mature branch, although the exact diameter yn 15294 (NY), 9
could not be traced. Authors be plant names are according TNAM "ania crassa A. C. Sm. 001 OMBIA. Cauca, J. L.
to Brummit and Powell (1992). Two samples were pre- Aueyn et al. 7378 (NY), 20 mm: M. ericae Sleumer:
served in FAA to investigate living substane es in fibers. ECUADOR. 5 J. I. Luteyn & M. Lebrón-
Institutional wood e used in this study are a Luteyn 5639 (NY), 15 mm: M. dl Benth.) A.
reviated according to the Index тйлй (Sissi: 1988). C. Sm.: COI a Cauca . Luteyn et al.
Other ое that were used to collect wood samples 7386 (NY), 13 mm; M. loeseneriana Hoerold: EC-
are The National Botanic Garden of Belgium (BR), The UADOR. Carehi, J. L. Luteyn & M. Lebrón-Luteyn
Royal ies D Edinburgh (E), and The New York 5726 (NY), 18 mm; M. mM Hoerold: COLOM-
Botanical Garden (NY). BIA. Valle, J. L. Lute ebrón-Luteyn 6957
(NY), 19 mm; M. rupestris (Kunth) A. C. Sm.: VE-

Chiriquí, J. /

—

Agapetes. flava (Hook. f.) Sleumer: BHUTAN. Chukka, .
Gri

4 NEZUELA. L. Williams 1 (Uw 35316), 18 mm:
rierson & D. Long 3076 (E 19822403), 10 mm: A. M. stricta A. C. OR. Carchi, J. /.

ii Diels: THAIL/ ies Seres d y B. J. teyn & M. p. Eod 5744 (NY), 10 mm.
Burtt 958 (E 19672592). 7 Ж: de Eon 8 chimantensis Maguire, Steyerm. & Luteyn: VE-
MYANMAR. V Kingdon- Ward 19097 (E 19: 500046). NEZUELA. Bolívar, O. Huber 9010 (NY), 7 mm.
10 mm: A. moorei Hemsl.: origin and collector un- Notopora cao A. C. un ih 'NEZUELA. Bolivar, J.
known (E 19696069), 10 mm; A. sikkimensis Airy E yn 9596 (NY). ] m; V. schomburgkii Hook.
Shaw: BHUTAN. Phuntsholing, /. peel & D. ЖУ UELA. 2 55 el at 5808 (Uw 27397), 10
Long 5778 (E 19842032), 12 mm; A

tegata С. mn
Don: INDIA. Meghalaya, D. E len deis 106(k Ore ew ensis Luteyn: ECUADOR. Loja, J. L.
19751313). 9 mm.

Luteyn 15394 (NY), 4 mm.
Anthopterus wardii Ball: COLOMBIA. Nariño, J. L. Lu- Orthaea на Га ECUADOR. Могопа- —
teyn & M. Le um agio 6865 (NY), 8 mm; A. wardii g „ Luteyn & M. Lebrón-Luteyn 5794 (NY),
Eres е . van Rooden et al. 443 (

Uw mm.
25586), 7 m Plutarchia ecuadorensis Luteyn: ECUADOR. Azuay, J. /
Cavendishia isse (J. St.-Hil.) Hoerold: BOLIVIA. La & M. Lebr sd Hun 5778 (NY). 13 mm; Р
az. L. J. Dorr et a 6890 (Lw), 12 mm; C. com- neun (Benth.) A. ln OMBIA. Cauca, J.
pacta А. C. Sm.: COLOMBIA. van Rooden et al. 555 ‚ Luteyn 10108 (NY, 5 m. |
(Uw 25619), 15 mm e callista Donn. Sm.: SURI- Polyclia turbinata (Kuntze) ri C. Sm.: BOLIVIA. Co-
NAM. Lely Mountains, Lindeman & Stoffers 502 chabamba, J. L. Luteyn 15453 (NY). 10 mm.
n 21835), 11 mm; C. lindauiana Hoerold: CO- Psammisia sp. indet.: COLOMBIA. van Rooden et al. 359
OMBIA. van Rooden et al. 630 (Uw 25642), 15 Jw 25565), 30 mm; P. pw e Hoerold: EC-
nm; C. pubescens (Kunth) er VENEZUELA. L. UADOR. Pichincha, J. L.

Williams 10020 (Uw 35101), 43 mm; С. و‎ ten 5621 (NY), 7 mm; A.
A. C. Sm.: COLOMBIA. van Pun et al. 371 (U ADOR. Maas et al. 3041 (Uw 23589). am mm; Р
25568), 21 mm. graebneriana Hoerold: COLOMBIA. Nariño, J. L.
Ceratostema торта (Sleumer) А. C. Sm.: ECUADOR. Luteyn & M. гб Luteyn 6809 (NY), 10 mm; Р.
soja, С. P. Lewis 3345 a aa 20 mm: C. re- gutanensis Klotzsch NEZUELA. Amazonas, В
ginaldii gen A. C. : EC Hera Loja, L. Maguire et al. 42397 (Tw 36530), 11 mm; P. gui-
J. Dorr & 1. Valdespino jur (Lw), 15 n anensis Klotzsch: ECUADOR. Azuay, Camp 4367
pon spectabilis Are A. - Sm.: PERU. Cuz- (Uw 10655). 11 mm; P penduliflora (Dunal)
2 (NY), 7 Klotzsch: VE NEZUE LA. Trujillo, J. L. Luteyn et al.
Dimorphanihera aiie g var. . collinsii INDO- TE (NY), 8 mm; P. cf. ulbrichiana Hoerold: EC-
NES an, — 4902 (Tw 23696), 60 mm: АРОК. Pichincha, J. L. Luteyn & M. Lebrón-Lu-
A ar J. Sm. var. cornuta: EAST NEW GUIN- pea 6532 (NY), 12 mm

35 mm; S. sp.

EA. Vink 17084 (Kw 11639, Uw 18298), 51 mm: d Satyria sp. indet.: COLOMBIA. Antioquia, J. L. Luteyn
dekockii J. J. Sm. var. pubiflora Sleumer: EAST NE et al. 7017 (NY), 16 mm; 5. sp. indet.: BRAZIL. В.
GUINEA. Vink 17307 (Kw 11639. Uw 18316). AS Maguire et al. 48650 (Uw 16976), |

592 Annals of the
Missouri Botanical Garden
indet.: BRAZIL. В. Maguire et al. 46784 (Uw 6 mm; ES о Marshall: U.S.A. Texas, H. No-
7005), 22 mm; S. sp. indet.: COLOMBIA. Antio- p 8 (Tw 18270). mature; V. atrococcum A. Heller:
quia, J. I. Luteyn & M. Le brón- Pan 7177 (NY Wire 0 8 unknown (kw 11706),

15 mm; 5. carnosiflora Lanj.: ZUELA. Ama-
zonas, B. Maguire et al. 42061 (Tw 36: 580), 15 mm;

S. meiantha Donn. Sm.: e D. e e
9746 (MADw 23933), mature; 5. panurensis (Meisi
Nied.: BRAZIL. B. Mea et al. 48650 0

S. warszewiczii Klotzsch: MEXICO.
Veracruz, | Cedillo & J. I. Calzada 170 (BR),
10 mm: S. warszewiczii Klotzsch: origin unknown,
Warszewicz, (BR), 12 mm.

Semiramisia 5 95 ve Sm.:

20301), N

COLOMBIA. Nari-

eyn 152 NY). 9 mm.
Siphon иб, а Kine he PERU. € g ү! J. L.
eyn & M. Lebrón- n yn 6377 (NY), 14 mm.

Shy rmum sp. indet.: ECUADOR. Pie Vul ‘ha, G.
gent (Е 19762390), w mm; S. buxifolium e j^
Endl.: ECUADOR. 6. V (E 19762390), 6 mm:
S. sodiroi A. C. Sm.: E ADOR. Pichincha, G. Ar-
gent 526 (Е 19762398), €

и racemosa (Vahl) Bu arn: : DOMINIC A. Chambers

2555 (Uw 15385). 22 mm.

Phemistoclesia d A. C. Sm.: COLOMBIA. A. M.
Cleef 2€ bru 20767). 5 mm: T. pendula Klotsch:
VENEZ "T La 1 Bret eler 3476 (Uw
11013), 11 5 T. vegas COLOMBIA,
Boyac ‚ Luteyn er al. 7500 (У Y. 13 mm.

Thibaudia angustifolia Hook.: Amazonas, J. L.

шеуп & ebrón-Luteyn 5. 528 (NY). 13 mm: T.
еды, НВК: ECU ADOR, ise hi, J. /
‚ Lebrón-Luteyn 5725 (N
inda h) Hoerold: VENEZL Е
0 et al. 27673 (Tw 36559). 20 mm; e es
. Blake: VENEZUELA. Mérida, J. L. yn el
al re (NY). 15 mm; J. martiniana 7 Sm.
ECUADOR. Pichincha, J. / teyn & M. ч и
Luteyn 5654 (NY). 24 mm: T. pac ori la A.
COLOMBIA. Cuatrecasas 19876 (Uw 1 11
mm; T. parvifolia Hoerold: COLOMBIA. ч auea, J.
L. Luteyn & M. Lebrón-Luteyn 6897 14 mm:
T. rigidiflora A. C. Sm: COLOMBIA. "Valle, L.
Luteyn & M. Lebrón-Luteyn 6985 (NY), 23 mn

Vaccinium sp. indet: U.S.A. Hawaii, W Stern 2980 (Tw
24148), 33 mm; V. rmm Britton: AFRICA. H.
Brown 52 (Kw 1170 70 mm: V angustifolium
Benth. (preserved in К b BELGIUM. n Lens (BR).

á

E

mature; V. bancanum Miq.: BRUNEI. Collector un-
known, (Kw 74737). 67 mm; P barandanum Vidal
var. ee Mp ur uns M. Jacobs 7249
(Uw 33743), 45 mm; V. berberidifolium (A. Gray)
: U.S.A. Stern &
18579), 9 mm; Y
Guangdong, ee Research Institute

| calycinum Sm.: U.S.A. Hawaii,
A 24121), 17 mm; V. шлш
‘OSTA RICA. San José, M. Wiemann 13
(Uw 30897 ), mature; V. corymbode dp Dun.: CO-
LOMBIA. J. ue m Е (Tw 20784), mature;
V. corymbosum Li: DA. Québec, R. Dechamps
5003 (Tw 33€ E m; V ае Vidal:
P ШТ INES. M. Jacobs 7270 (Uw 33746), 36 mm;
V. exaristatum Kurz: INDIA. Жн. Lushai Hills,

. E. Parry 45 (Kw 167 5 }. 36 mm: V. exul Bolus:
SoU TH AFRICA. J. Prior 464, 23 mm; V. 17

O. Williams) Wilbur & Luteyn: PANAMA. Chi-
шш Maas et al. 4957 (Uw 26277), 33 mm; е, flo-

bracteatum T

—
=
Y.
=
=
— „
Е
N
PS
o
za
m~
~
—

8
E
~

Je ا ا‎ : BR), 5 mm:
\. Washington, H. Dechamps 4460 (Tw 4

fi 5 mm; К leschenaultii Wight: INDIA. Collector un-
known (Kw 70598), mature; V. leucanthum Schltdl.:
MEXICO. Puebla, L. Lebacq 73 (Tw 24590), adult:
V maderense Link: SPAIN. Madeira, V. H. Mason
W 11745), mature; V. membranaceum Hook.:
S.A. Oregon, R. Pechamps. m 5 (Tw 16029), 9
mm; V. meridionale Sw.: LA. L. Williams
10896 (Uw 35314), mature; V aes t L.: BEL-
GIUM. Luik, A. Duo (Tw 43142), 8 mm; V.
occidentale A. Gray: U.S.A. Oregon, К. e
1414 (Tw 46260), mature; V. ovatum Pursh: A.
Oregon, K. Dechamps 4418 (Tw 46267). 23 mm; ү
a ai Sm.: U.S.A. Oregon, R. Dechamps 4310
(Tw 45996), 27 mm: V. puberulum C. К. W. Meissn.
M: guire, Steyerm. &
GUYANA. Maas et al. :

var. subcrenulatum

5 Leiberg: U.S. LA. Oregon, К. Dechamps
383 (Tw 46187), 6 mm; V. stanleyi Schweinf.: DEM-
oc RATIC REPL iia IC OF CONGO. fle. P. Deuse
(BR), 9 mm: V. uliginosum lL: NORWAY. Hor-
1 R. Dechamps 6033 (Tw 38581). 6 mm.

REVISION OF DRACONTIUM
(ARACEAE)!

Guanghua Zhu? and Thomas B. Croat?

ABSTRACT

A taxonomic revision of the genus ن‎ L. (Araceae) is prese ented pre pes) J morphological, anatom-

ical, and phytogeographic data. Dracontium is treated as comprising 23 species, incluc 10 new species: D. ama-
zonense G. Zhu & Croat, D. enga G. Zhu & Croat, D. 5 % Zhu & са D. bogneri G. Zhu &
Croat, D. grandispathum G. Zhu & Croat, D. ip dnd G. Zhu & Croat, D. ия G. Zhu roat, D.
ран G. Zhu & Croat, D. cd G. Zhu & Croat, and D. prancei c. "ma & . Five names are new s"
lectotypified herein: Amorphophallus а Lem., A. papillosus hort. ex Rafarin, e ntium gui rus rs, D.

Engl. and D. soconuscum Matuda. The following species are newly synonymized: D. carderi Hook. f., D. costaricense
Engl., D. dressleri Croat, D. lineare G. S. Raine & Tillett. D. loretense K. Krause, b ornatum K. ен D. trianae

E bal. . and Echidni
Key words:

пит regelianum Enel.

All taxa are described and illustrated.
Araceae, Dracontium, monograph, taxonomy,

The Araceae are a family of herbaceous mono-
cots with 106 genera and approximately 3500 spe-
cles, the vast majority occurring in the New World
tropics (Croat, 1988, 1992). The World Checklist
and Bibliography of Araceae (and Acoraceae) lists
a total of 2824 recorded species (Govaerts & Fro-
din, 2002).

verse

Members of the family are highly di-
life form, leaf morphology, and inflores-
cence characteristics. Life forms range from
free-floating aquatics to terrestrial
(sometimes tuberous), epiphytic or hemiepiphytic

plants, to climbers. Leaves range from simple and

submerged

entire to compound and highly divided, and may
be basal or produced from an aerial stem. The fam-
ily is best characterized by its distinctive inflores-
cence, a spadix with bisexual or unisexual flowers
(sometimes with a sterile region) subtended by a
solitary pedunculate spathe.

The present study of Dracontium L. comprises a
taxonomic revision of one of the most poorly known
tuberous genera in the Araceae. Dracontium, as
here recognized with 23 species, represents the
most species-rich tuberous genus of the Araceae in
the New World. it shares a great sim-
ilarity with the Old World genus Amorphophallus
Blume ex Decne. Plants in both genera usually con-

Vegetatively,

sist of a single leaf arising from an underground
tuber with a more or less mottled, reptilian-pat-
terned petiole up to several meters long with a
highly divided, compound, spreading blade reach-
ing as much as three meters or more in diameter,
Inflorescences of both genera are notorious for their
fetid scents at anthesis. However, Dracontium dif-
fers sharply from Amorphophallus in having bisex-
ual flowers on a uniform spadix.

ссига!е identification of Dracontium species
has been difficult because of the paucity and in-
adequacy of herbarium material and their sporadic
phenology. Herbarium specimens, though compar-
atively abundant for some species such as Dracon-
пит spruceanum (Schott) G. Zhu, are frequently
sterile and often incomplete since mature adult
leaves are almost always too large to be mounted
on a single herbarium sheet. Frequently, a single
leaf is mounted on several to many herbarium
sheets. Hence, intensive study of living material in
the field or under cultivation is essential. Though
local populations may contain many plants, popu-

ations of Dracontium are often widely scattered
and single individuals not frequently encountered.
Under unfavorable growing conditions, plants of
Dracontium may remain vegetative for many years,

s. Many indiv idual

m

he University of Missouri-St.
i k. Mi ce €:
Keating, Petra Schmidt, Emily Yates, Dan Nicolson, Mic
Werff, and Scott Zona for providing
following he rbaria for providing loans of specimens
+ IBE, INB, INPA, JAUM, K,
SP. TRIN, TULV, U,

grant DE B-931017 n an gia 55 the pun ia ps Tropical е а! 4 M
sity of Missouri-St.

Fellowship. A teaching assistantship from ie
Ке ‘llowship provided partial financial suppo
Missouri Botanical Garden,

Ini ver

ANN. Missouni Bor.

s revision is based on a study complete das a ги fulfillment of a Ph.
s have contrib
каушп,

М, MENG, MG. M
JS.

D. degree in biology for the first author
We thank John Banta, Josef
. Victoria ee Richard

Haus Vissers, Henk van der

uled to the study.

Richardson,

plant mate Hal and E Apful communications. We also thank de curators of the
/ BM, |

‚ BBS,
‚ МЕМ, and W

Louis and an ae ew W. Mellon Fandi АМ

P.O. Box е. St. Louis, Missouri 63166-0299, U.S.A.

GARD. 91: 593-667. 2004.

594

Annals of the
Missouri Botanical Garden

and often go dormant for two г four months in the

dry season. Inflorescences of Dracontium often
arise from the apex of the Ше before or after leaf
development. Therefore, matching fertile with ster-
ile herbarium material of the same Dracontium spe-
cies is often problematic.

ive plants of Dracontium are not uncommon in

cultivation in botanical gardens and aroid nurser-
ies, as they share an ornamental appeal with Amor-
phophallus species and are easy to propagate and
maintain. Unfortunately, cultivated material of Dra-
contium is limited to only a few species, such as
D. gigas (Seem.) Engl., D. polyphyllum L., and D.
spruceanum. Locating these plants in the field

often not difficult since populations of Dracontium
are usually well known to native people due to the
distinctive, reptilian-patterned petioles and medic-

inal uses.

MATERIALS AND METHODS

This revision was conducted mainly at the Mis-
souri Botanical Garden, where the largest living
and herbarium collections of Dracontium in the
world are housed. Field research for this study was
conducted in Costa Rica, Panama, and Brazil be-
tween 1992 and 1995. Trips were made to several
botanical gardens to study cultivated plants, in-
cluding the Marie Selby Botanical Gardens and The
New York Botanical Garden in the Unites States,
and the Sao Paulo Botanical Garden and Botanical
Garden of Rio de Janeiro in Brazil, as well as to
herbaria CR, К, GH, HB, IAN, IBGE, ISC, a

PMA, R, RB, SCZ, SEL, SP, SPSF, UB, UEC, US,
and WSU. Over 670 collections comprising about
3000 herbarium sheets, including loans from 49
major institutions worldwide, were studied (see Ap-
pendices 1, 2). Data from all cited specimens are
recorded in the Missouri Botanical Garden data-
base TROPICOS.

In this study, we have relied heavily upon live
collections, especially the second author's gatherings
during his more than 35 years of fieldwork in the
Neotropics. Some spec ies, such as Dracontium gui-
anense G. Zhu & Croat, are known only from a few
herbarium collections. In such cases, descriptions
are from herbarium specimens only. Due to the rarity
of many Dracontium species, all specimens with
proper collecting information are cited, including
those prepared from cultivated plants. For species
determinations, we have also relied on photographs
prepared by Croat and many other individuals to
reconstruct the natural habits for these plants.

Descriptions of species were prepared using the

DELTA (DEscriptive Language for TAxonomy) pro-

gram (Dallwitz et al., 1995). The program TAXA-
SOFT (Gouda, 1994) was used for data mainte-
nance of DELTA.
prepared by using TROPICOS. Ecological zones
are estimated by using the Holdridge Life Zone sys-
tem (Holdridge et al., 1971)

Material for chromosomal studies was obtained

The exsiccatal information was

from plants cultivated at the Missouri Botanical
Garden. Growing root tips were treated in 0.002M
8-hydroxyquinoline for 4 hr. before being fixed in
ethanol-glacial acetic acid-chloroform (6:3:1) at
8°C overnight. Root tips were then rotated through
a hydrated 70%-50%-25%-10% ethanol series,
were macerated with IN НСІ (room temperature)
for 10 minutes, IN НСІ (60°C) for 8 min., and IN
НСІ (room temperature) for another 10 min., and
rinsed with deionized H,O for 30 min. before being
stained i in 0.5% Feulgen for 1.5 hr. (Masahiro Tak-

‚ pers. comm.). Finally, the plant material was
1 with deionized water, and slides with the
chromosome squashes were prepared.
TAXONOMIC HISTORY

The first mention of a species referable to Dra-
contium appeared in Hermann's Paradisi batavi
prodromus (1689: 315) as "Arum polyphyllum, dic-
tum Dracontium, caule scabro punicante, surina-

s.

mense” and “Dracontium americanum caule scabro
puniceo radice Cyclaminis.” The plant was intro-
duced into the gardens of Holland by the early
Dutch plant-hunters from Surinam in the second
half of the 17th century. A corresponding plate was
ater published by Plukenet (1696, t. 149, fig. 1) in
his Almagestum under the name “Arum polyphyl-

lum surinamense caule atrorubente glabro et ele-

ganter variegato.” This same species was rede-
scribed by Hermann (1698: 93-94) in his
Paradisus batavus as “Dracontium americanum

scabro puniceo caule radice Cyclaminis,” along with
t. 93) under the name “Arum polyphyllum

caule scabro punicante.” Linnaeus (1737) published
the first comprehensive description of this species

—

a figure

after he personally studied a flowering specimen in
the Clifford Garden at Hartecamp, Holland. Later,
he validly published the genus Dracontium with
five species in Species Plantarum and established
the binominal Dracontium polyphyllum (Linnaeus,
1753), which is the only species still recognized
within Dracontium. Under D. polyphyllum, |
us (1753: 967) cited both Plukenet’s and Her-
was later selected

Annae-

mann's figures. Hermann's figure
as the lectotype of D. polyphyllum (Hay, 1992).
Since D. polyphyllum was referred to as
by Britton and Wilson (1923: 130), it was accepted

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

as the generic type of Dracontium (Jarvis et al.,
1993: 43)

Rafinesque (1838: 12-13) evidently misidenti-
fied a plant as D. polyphyllum saying “the scandent
sp. appear the type of Dracontium, which Anderson
and
superfluously renamed D. polyphyllum as Eutereia

changed to Mostera perhaps a better name.”

nigricans Rafinesque. Therefore, the generic name
Futereia is a superfluous name for Dracontium.
The genus Dracontium remained known only
with from Surinam until Richard
Schomburgk’s expedition to Guyana (1840-1844).
during which he collected a second species of the

one species

genus. Several living tubers of this species were
sent to the Botanical Garden of Berlin, Germany,

1843 (Roth. 1922, 1923: Zhu et al.. 1998). This
species was later described by Kunth (1844) as D.
dubium Kunth. Schott (1857b) transferred this spe-
cies to his newly described genus Echidnium Schott
and created a superfluous name, E.
Schott (Zhu et al., 1998).
(1857b). distinguished

from Dracontium by having a unilocular ovary with

schomburgkii
According to Schott
Echidnium is ostensibly
two ovules, as opposed to a bi- or pluri-locular ova-
ry in Dracontium.

When describing the single species in his new
genus Ophione Schott, Schott (1857a) described a
third species of Dracontium as O. purdieana Schott.
which differs from Echidnium in having an ovary
with 4 to 5 locules, and from Dracontium in having
a long-acuminate spathe. Later, Schott (1858a) de-
scribed another Dracontium species as Echidnium
spruceanum Schott before publishing the first com-
prehensive classification of the Araceae ii
Prodromus systematis aroidearum in 1860,
laid the foundation for the modern generic concepts
within the aroid family. In his Prodromus (1860).
Schott recognized four Dracontium species in three
genera, namely Dracontium, Echidnium, and Ophi-
one, Classified along with Symplocarpus Salisbury

the

~

which

in Araceae subtribe Dracontiinae next to subtribe
Lasiinae in the tribe Orontieae: Dracontium poly-
phyllum, Echidnium schomburgkii, E. spruceanum.
and Ophione purdieana. The superfluous name Ё.
schomburgkii was used for D. dubium (Zhu et al.,
998). The diagnostic features used by Schott
(1860) for his separation of these genera were
based exclusively characters. such
spathe and spadix shapes, tepal number and shape,
stigma lobes, ovary number and shape. and number
of ovules per locule. All these characters may be
useful for the separation of species within the

on [floral as

group, but not for defining generic boundaries.
Unable to confirm the characters of unilocular
ovary with two ovules for Echidnium and the im-

portance of the floral characters, Engler (1889)
transferred Echidnium as a section to Dracontium
while recognizing Ophione, but later revived the ge-
neric status of Echidnium in his Das Pflanzenreich
1911) and synonymized Ophione within Dracon-
tium. Bogner (1985) and Hay (1988) noted that a

unilocular ovary with two ovules cannot be used as

pe
—

a generic character in this group and once again
synonymized Echidnium within Dracontium. The
supposedly unilocular ovary with two ovules of H.
dubium (Kunth) Engl. is erroneous based on its
1998), as well as the type of
1996).

not occur in Dracontium and this genus never has

пеоіуре (Zhu et al.,
E. spruceanum (Zhu, Unilocular ovaries do
more than one ovule in each locule: these stand as
(Zhu. 1995, 1996: Zhu
1998). Echidnium spruceanum Schott was re-
cently transferred to Dracontium by Zhu (1996).
Koch (1859) described a fifth species, D. asper-
um K. Koch, from a plant cultivated at the Berlin
Botanical. Garden.

generic traits of the genus
et al.,

This plant had been obtained
from the Botanical Garden in Amsterdam and orig-
inated from Surinam (Koch, 1859). This species
was apparently unknown to Schott in 1860. Be-
cause of the same country of origin and the ambig-
uous original descriptions, especially the use of an
unreliable diagnostic for petiole texture, D. asperum
had been confused with D. polyphyllum for centu-
1995).
applied indiscriminately and have been used in dif-
ferent senses by different authors (Schott, 1858b:
Engler. 1878, 1911; Jonker-Verhoef & Jonker.
1953). Specimens of the same taxon have been
identified with either name in herbaria throughout

ries (Zhu & Grayum, The names have been

the world. Through lectotypification and neotypifi-
cation, Zhu and Grayum (1995) elaborated the con-
cept of these two species. Dracontium asperum has
spathe margins broadly overlapping and seed with
a strongly interrupted dorsal ridge, while D. poly-
phyllum has spathe margins rarely overlapping and
seed with a continuous dorsal ridge.

In 1865, Schott described the genus Chersy-
drium Schott on a single species, C. jararaca
Schott. citing D. asperum as a synonym (Schott.
1865: 73).

iole armament is a variable character in Dracon-

In the protologue, Schott noted that pet-

tium, but failed to provide any diagnostic for his
new Chersydrium. Because D. asperum was cited as
a synonym, according to the Code (Greuter et al.,
2000, Art. 52.1) Chersydrium jararaca is superflu-
ous, illegitimate, and to be rejected. Berthold See-
mann (1869) described a new genus, Godwinia
Seem., from Nicaragua with a single species, G.
gigas, in honor of George Godwin. Masters (1873)
later published a drawing of an inflorescence of G.

Annals of th
Missouri Botanical Garden

gigas and suggested the species would be more
properly placed in the genus Dracontium, but he
did not make the transfer. Engler (1877) agreed,
and two years later (1879) established the combi-
nation D. gigas (Seem.) Engl., which synonymized
Godwinia. An epitype, an interpretative type when
all original material is demonstrably ambiguous
(Greuter et al., 2000, Art. 9.7), represented the first
axonomic application of the concept in seed plants
and was designated for the species by Zhu (19944).

In his first classification of the family Araceae,
Engler (1877) introduced his subfamily concepts
with all presently recognized Dracontium species

-
—

in subfamily Lasioideae, which is defined by assim-
ilated leaves that persist for only one vegetative
season. Dracontium remains a member of subfamily
Lasioideae, although the modern classifications of
the Araceae differ radically above the tribal level
(Grayum, 1990; Bogner & Nicolson, 1991; Mayo et
al., 1997; Keating, 2004). Following Engler (1877,
1920), in the tribe

Lasieae when tribes are recognized in the subfamily

Dracontium has been treated

asioideae (Hay, 1992).

In his infrageneric classification, Engler (1889)
recognized three sections: Dracontium sect. Eudra-
contium, including D. polyphyllum and D. asperum,
characterized by a very short peduncle 5-18 cm
long above ground and a relatively small spathe
(6)10—20 em long; Dracontium sect. Godwinia, with
the single species D. gigas, with its long peduncle
to 30-120 ст long and a relatively large spathe to
58-78 cm long; and Dracontium sect. Echidnium,
presumably with a unilocular ovary, which was
proven to be erroneous (Zhu, 1996).

Demonstrating his extraordinary knowledge of
the Araceae, Engler (1905) described D. longipes
and D. pittieri from Brazil and Costa Rica, respec-
tively. In 1911, he published the only extant revi-
sion of the genus synonymizing Ophione and rein-
stating Echidnium. Twelve names in three genera
were recognized: Crytosperma spruceanum (= D.
spruceanum); Dracontium asperum, D. cardert, D.
costaricense, D. longipes, D. polyphyllum, D. pur-
dieanum, and D. trianae in section Eudracontium:
D. gigas and D. pittieri in section Godwinia; and
Echidnium dubium and E. regelianum. Ten of these
species remain recognized in Dracontium.
1911.
more names under Dracontium have been pub-
lished. Dracontium ulei К. Krause was described
from Acre, Brazil (Krause, 1914). Dracontium so-
conuscum Matuda was described from southern
Mexico (Matuda, 1949). Dracontium dressleri Croat
was described from Panama and was named in hon-
or of Robert Dressler (Croat, 1975). Dracontium

Since Englers landmark work in eight

margaretae Bogner was described from Mato Gros-
so, Brazil, and was named in honor of Margarete
Three species were de-

—

Emmerich (Bogner, 1981
scribed by Bunting in 1986 and 1988, D. aricuais-
anum G. Bunting, D. changuango G. Bunting, and
D. lineare G. Bunting. Finally, D. croatii G. Zhu
was described from the Andes in honor of Thomas
Croat (Zhu, 1995).

Herein, 10 additional species are described:
Dracontium amazonense, D. angustispathum, D. as-
perispathum, D. bogneri, D. grandispathum, D.
grayumianum, D. guianense, D. peruvianum, D.

plowmanii, and D. prancei.

MORPHOLOGY AND ANATOMY

TUBERS, TUBERCLES, AND ROOTS

Tubers (Fig. 1).
ogy of tubers vary from one season to the next.
Starch accumulates in the tuber to its maximum
prior to inflorescence development, and is for the

The size, weight, and morphol-

most part utilized during production of the inflo-
rescence and new leaf. Diminution of the tuber is
often associated with a change in its vertical depth
rather than the horizonal diameter of the tuber.
Since the tuber dimensions vary seasonally, hollow
spaces in the soil are often seen both above (1—3
em) and below (3-8 cm) the tuber.
space accommodates the growth of tubercles and

This upper

contractile roots, while the lower hollow allows the
tuber to settle deeper into the soil as the contractile
roots dry out during dormancy. This settling may
gain protection from corm-eating herbivores such
as agoulis and peccaries. However, disturbances
from these same animals are responsible for dis-
tributing the tubercles.
Tubercles (Fig. 1).
of tubers, rarely on the side of irregularly shaped
tubers in D. margaretae, and often mixed with
Tubercles allow Dracontium to reproduce
vegetatively. They
only after disturbance. When a tuber is disturbed
or broken off, tubercles start to change in shape.
somewhat irregularly shortening, and produce their

Tubercles are borne on top

roots.
are usually dormant, activated

own shoot and roots.

Roots (Fig. I). Primary roots of Dracontium em-
anate from the flattened apex of the tuber and grow
downward in all directions, completely surrounding
the tuber (Fig. IB). Secondary roots start below the
tuber apex and are subdivided into many smaller
roots. The strong and often contractile root system
functions not only in water and nutrient absorption,
but also serves to support the plant. The roots hold
the tuber in a position that facilitates the formation
of the hollow spaces above and below the tuber.

597

Zhu & Croat

Volume 91, Number 4

2004

Revision of Dracontium

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598

Annals of the
Missouri Botanical Garden

The tuber naturally assumes a deeper position
when the roots dry out after each growing season.

LEAVES

Cataphylls. Саарһу are the bract-like struc-
tures subtending the petiole, and usually complete-
ly embracing new growth from tubers after dorman-
cy, oflen drying long before the leaf blade fully
expands, and usually rotting away, becoming barely
visible after the leaf blade has fully expanded.

Petioles (Fig. 2).
are thick and aerenchymatous (Fig. 2A), frequently
more than 2 m long. The exterior surface is often
highly variegated (Fig. 2A, В), dark
green, sometimes brown tinged, mottled with pale

The petioles of Dracontium

or purplish

green or creamy areas suggesting a reptilian pattern
(Fig. 2A, B). The mottled areas often appear as up-
ward brush strokes, which originate from protuber-
ances. Petiole surface texture is variable among
species, from smooth textures to heavily beset with
protuberances (Fig. 2B). The latter are often accom-
panied by horizontally elongate, irregular projec-
tions. bordering two differently colored areas and
sometimes also by spiny projections to 2 mm long.
The proximal half of the petiole tends to have more
protuberances or projections, while the distal half
is much smoother. The aerenchyma cells of the pet-
iole are cylindrical, hollow, to 6 em long and 0.5
cm wide (Fig. 20). The sheathing of the petiole is
convolute, forming a closed space in the center
through which the inflorescence or leaf initiates.
Blades (Fig. 2D). The tripartite leaf blade is
held horizontally or ascending up to 45? from the
petiole apex. Blade rachises may be mottled similar
to the petioles but in much paler shades or may be
concolored (Fig. : They are usually smooth but
may be armed with spiny projections, also similar
to those of the petiole. The basal rachis of the mid-
dle blade division may be as long as the lateral
divisions (D. spruceanum) or twice or more as long
as these (D. angustispathum and D. grayumianum).
Segments of Dracontium leaf blades can be entire

or lobed, and can be distinguished on the basis of

their position. Sometimes, there are rounded, tri-
angular, or oblanceolate contrastingly small seg-
ments among the basal and medial segments. These
small segments may be absent (D. spruceanum) or
alternate with the larger segments (D. soconuscum),
or more often found near the base of each leaf di-
vision (D. polyphyllum). They may be confluent
with larger segments (D. gigas) or free (D. spru-
ceanum). Likewise, medial and basal segments may

be confluent or free from one another. The basal

subdivisions of Dracontium consist of many smaller

segments (D. gigas and D. grayumianum) or some-
The

terminal subdivisions always consist of at least two

—

times a single segment (D. angustispathum).

segments in the lateral division and at least three
segments in the middle division.

In the early development of a Dracontium leaf
blade, all leaf divisions may point upward (D. gi-
gas, Fig. 11A; D. Fig. 16B), or the
middle divisions may point upward while the lateral
divisions point downward (D. asperum; D. spru-
ceanum, Fig. 25A). Juvenile leaves of Dracontium
are usually sagittate or sagittately lobed, rarely lin-
ear or trifid (D. margaretae).

margaretae,

INFLORESCENCES

Bracteoles (Figs. 4A, 4B, 8A, 16C, 17B,
24B). Bracteoles are the bract-like structure sub-
tending the peduncle of each Dracontium inflores-
cence. The relative length of the innermost (also
the longest) bracteole to the peduncle is an impor-
tant character
tium. It ranges from being much shorter than the
peduncle (D. plowmanii) to longer than the pedun-
cle (D. prancei). The bracteoles usually rot away
soon after anthesis.

Peduncles (Figs. ТА, 8A, 11B, 13А).
Dracontium inflorescences are produced before, or
sometimes after, new leaf development. When in-
florescences are produced right after a new leaf,
they often appear as having developed simulta-
neously with the leaf, as sometimes in D. croatii,
D. pittieri, and D. spruceanum (Fig. 25A). The fer-
tile peduncles of Dracontium are usually shorter
and thinner than the associated petiole and may be
completely underground (D. dubium) or nearly as
long as the petiole, rarely exceeding the petiole (as
sometimes in D. spruceanum). Peduncles are much
like the petioles in terms of coloration and arma-

distinguishing species in Dracon-

ment.
Spathe (Figs. 4A, 4B, 7A, 9A, 9B).
and size of the spathe distinguish species of Dra-

The shape

contium, perhaps more so than any other character.
The spathe is marcescent and often disintegrates
on a developed infructescence. At anthesis, the
length of the spathe in the genus may range from
a few ст long and 1 cm wide as in D. bogneri to
as much as 85 cm long and 20 em wide as in D.
gigas. Spathes may be more or less hooded and
boat-shaped (D. asperum, D. gigas, and D. pittieri)
or suddenly contracted at a certain point and grad-
ually acuminate distally (D. angustispathum, D. du-
bium, D. purdieanum, and D. spruceanum). The
spathe margins may be broadly overlapping near
the base forming a bell-shaped tube and broadly

Volume 91, Number 4 Zhu & Croat 599
2004 Revision of Dracontium

Figure 2. A-D, Petioles and blade. —A. Dracontium grayumianum (G. Zhu & Croat 1506). Close up of petiole
showing variegation. —B. D. croatii (Croat 72368 pius 's showing vi ее and short spines. —C. D. gigas .
E. 1156). н ss showing exterior surface and inner surface with aerenchymatous cells. — p. D. atii (Croat

2368). Lower surface of leaf blade showing the prominently round-raised medi: il ribs and pinnately lobe ^ la ateral veins.

600

Annals of the
Missouri Botanical Garden

open above as in H. grayumianum, D. purdieanum,

and D.
lower % to % with only a narrow opening above (D.

soconuscum. They broadly overlap at the
gigas and D. prancei), or barely overlap (D. pittieri
and D. polyphyllum). The apex of the spathe is var-
tably acuminate and ranges from erect or slightly
arching as seen in D. angustispathum, D. poly-
phyllum, and D. spruceanum to strongly arching to
perpendicular in D. amazonense and D. asperum.
The outer surface of the spathe is often matte,
with many elongate clumping projections. The
spathe may be maroon, tinged green (D. sprucean-
um), purplish red or olive-brown (D. polyphyllum),
green (D. croatii and sometimes D. spruceanum), o
sometimes with a basal paler area on the abaxial
D. asperum). The inner surface may be glossy

—

side
(D. angustispathum and D. plowmanii) or semiglos-
sy (D. gigas and D. pittier) or covered with densely
overlapping translucent scales (D. dubium and D.
purdieanum). Spathe inner surface is maroon (D.
polyphyllum), maroon tinged reddish (D. asperum
and D.
brown (D. spruceanum). There is usually a creamy

soconuscum), or reddish brown to olive-
white translucent area at the spathe base that may
be obscure (D. asperum, D. polyphyllum, and D.
ulei) or to l to 3 times as long as the spadix
height (D. asperispathum, D. grandispathum, D. pit-
пегі, and D. spruceanum). The inner surfaces of the
spathe are often covered with whitish or brownish
spotted. gland-like structures associated with the
stomata. These structures appear to control the
emission of scent (see section on Phenology and
Pollination).

райх (Figs. 3D, 4C, 7B, 11C).
Dracontium is sessile, or stipitate to 0.5-2.5 cm
long. It ranges from 1 to 9 em long and 0.5 to 2
em diam. at anthesis, and from 4 to 25 cm long
and 4 to 10 em diam. when fruiting.
the spadix corresponds to the color of the tepal api-
ces and styles, which may be dark purple. green.
light brown, or rarely gray. The spadix may be hid-
den at anthesis (D. croatii, Vig. OA, D. gigas, D.
spruceanum, and D. asperum) or exposed naturally
(D. polyphyllum, Fig. 21A. D. pittieri, D. soconus-
cum, Fig. 24A, D. purdieanum, Vig. 23A, and D.
dubium). A spadix may be typically cylindric (Fig.
11C), rarely globose, or sometimes cylindroid-ta-
pered (Fig. 22B). Sometimes 1 to 5 tepals at the
apex of the spadix are elongated into 0.5-1 cm ap-
pendages (D. dubium, D. grayumianum, D. pur-
dieanum, and D. soconuscum, Fig. 3D). The func-

tion of these appendages is unknown. The central

axis of the spadix consists of aerenchyma, similar

to those seen in the petioles and. peduncles.

The spadix of

The color of

FLOWERS

The flowers of Dracontium are arranged spirally
on the spadix. Each consists of a perianth, a single
pistil, and 4 to 19 stamens (Fig. 3B, C). The peri-
anth consists of 4 to 8 fornicate tepals that envelope
the pistil and stamens at anthesis. The apices of
the tepals are green to purple and covered with
yellow-tinged raphide cells. The lower portion of
each tepal is often transluscent, white to light
brown, sometimes with red or red-purple dots.

Stamens (Fig. 3C).
often slightly dilated, sube

Ds filaments are elongate,
ed, and abruptly

contracted at the apex into the connective. The an-
thers exceed the connective and are linear-elliptic
in shape. They are often yellow, turning reddish
brown, sometimes with dark purple, especially near
the aperture, after anthesis. The anthers are usually
hidden before anthesis and dehisce apically by a
vertical slit with a more or less rounded aperture
at anthesis (Fig. 26B). Pollen emerges from these
apertures in a strand that reaches the stigma, and
is as long as or longer than the style. The function
of these pollen strands is discussed in the section
on reproductive biology.

Pistils (Fig. 26А).

are narrowly ovoid, pale green, and incompletely 2-

The ovaries in Dracontium

to 5-loculed, with axile or basal placentation. The
ovules are solitary in the locules and amphitropous

r campylotropous. The style is 0.5-5 mm long

~

above the tepals at anthesis. It is dark purple to
pale green, and persistent or caducous. The stigmas
(Fig. 26А) are unlobed or variably up to 4-lobed,
usually covered with a translucent sticky liquid at
afterward. Ovaries are

anthesis but drying out

ovoid, pale green, incompletely 2- to 5(7)-loculed
with axile or basal placentation. Ovules are one per

locule, amphitropous or campylotropous.

FRUITS AND SEEDS

Fruits. The berries of Dracontium may be glo-
bose (D. eroatit, Fig. 9C; D. spruceanum), angularly
subglobose with three to six angles (D. grayumian-
um, Fig. 13C; D. longipes, Fig. 15B); or elongate
with a projection (D. angustispathum). They range
from having one seed (D. angustispathum) to as
many as seven seeds (D. polyphyllum). The young
berries are usually green, while the mature berries
may be orange (D. angustispathum, D. dubium, D.
croatu, D. gigas, D. grayumianum, D. peruvianum,
D. pittieri, and D. spruceanum), purple tinged (D.
asperum), green tinged purple (D. bogneri, D. po-
lyphyllum), red or purple-red (D. margaretae and
D. purdieanum), or bay brown (D. soconuscum

and sometimes D. gigas). The berries are usually

Volume 91, Number 4
2004

darker apically and may be depressed around the
persistent style (D. bogneri, D. dubium, and D. so-
conuscum) or rounded (D. angustispathum and D.
spruceanum). The berries are often covered with
small whitish raphide cells and sometimes. red
dots.
Seeds.

seed morphology, and this is of great value for spe-

Dracontium shows

great diversity ii

cies distinction in the genus. Seed size ranges from

3 mm wide (D. bogneri) to more than 11 mm wide

(D. croatit and D. peruvianum) with only a trace of

endosperm present. The seeds may be rounded (D.
croatit, D. gigas, and D. pittieri), elongate (D. spru-
ceanum and D. grayumianum), reniform (D. poly-
phyllum and D. plowmanii). or more or less trian-
gular (D. asperum). They are more or less laterally

compressed, with the sides either convex (D. po-

lyphyllum) or depressed (D. asperum). The sides of

the seeds may be smooth (D. polyphyllum, D. as-

and D. bognert) decorated with small

perum.
wart-like projections (D. spruceanum). The seeds
typically have three dorsal ridges (D. gigas. D. pit-
and D.
sometimes have only one (D. polyphyllum. D. as-

tieri, D. peruvianum, spruceanum), but
perum, and D. plowmanit) or none (D. bogneri). The
dorsal ridges may be continuous (D. polyphyllum
and D. plowmanit) or strongly interrupted (D. du-
bium, D. croatit, and D. grayumianum). and either
thin (D. grayumianum) or thick (D. croatit. D. gi-
gas, and D. peruvianum).

CHROMOSOME NUMBERS

All species of ре age that were examined
are diploids with 2n = 26, the only number known
in the tribe Lasieae (Petersen, 1989). These counts
of 2n = 26 were confirmed by the first author in
D. amazonense (G. Zhu 1454). D.
1267). D. polyphyllum (Croat 74210),

cei (Croat 73867), using the method mentioned in

gigas (Bogner

—

and D. pran-

Petersen (1989). Counts were made from root tips
in all cases. Dracontium has comparatively small

chromosomes, similar to those of other members of

the same tribe. Petersen (1989) showed that chro-
mosome size and number are highly variable in the
Araceae and of great importance for their taxonomy
and evolution at the generic level. However, based
on the Dracontium chromosomes seen thus far, thev
appear to be of little taxonomic value at the specific
level owing to their similarity in number, size, and
shape.

DISTRIBUTION AND HABITATS

Distribution. Species of Dracontium occur from
15°22’N latitude in the Mexican district of Socon-

Zhu & Croat 601
Revision of Dracontium

usco in Chiapas State (D. soconuscum), south
through Nicaragua, Costa Rica, Panama, the Do-

minican Republic and Puerto Rico, Colombia, Ve-
West Indies.
uador, Peru, Bolivia, and Brazil to the Tropic of

nezuela, Trinidad, the Guianas, Ec-
Capricorn in Paraguay. In South America, the east-
ern limit of the collections is 44°28'W longitude in
Brazil;

the Pacific coast of Colombia, Ecuador.

Maranhao, Dracontium extends west along
and Peru.
No collections of Dracontium are known from Cuba,
Chile.

Five species occur in Mesoamerica: Dracontium

Argentina, or Uruguay.
gigas, D. grayumianum, D. pittieri, D. soconuscum,
and D.

only species known from Mexico and the northern-

spruceanum. Dracontium soconuscum is the
most species of the genus. This species also occurs
in Costa Rica and Panama, and is very likely to
occur also in Guatemala, El Salvador, and Nicara-
eua. Dracontium gigas is the only species known
from Nicaragua: it is also known from the Atlantic
slope of Costa Rica in the provinces of Alajuela.
Heredia, and San José. All Mesoamerican species
besides H. grayumianum occur in Costa Rica, in-
cluding D. pittieri, endemic to the Pacific slope in
the province of Puntarenas. It has not been col-
lected in adjacent Panama, where three other spe-
and D.

has its

cles occur, D. soconuscum, D. spruceanum,

grayumianum. Draconttum soconuscum
southern geographic limit in the Panama Canal
area; to the south it is replaced by D. grayumian-
um. which has a typical Caribbean/Chocó distri-
bution pattern as encountered in Philodendron spe-
1996).

Dracontium spruceanum is the most widespread
Rica.
into northwestern Ec-

Andes

Peru, and northwest-

cies (Grayum,

species of the genus, ranging from Costa

through Panama, Colombia,
uador and along the eastern slope of the
through Amazonian Ecuador,
ern Amazonian Brazil. It is the only species of Dra-
contium that occurs on both slopes of the Andes,
having been collected on the western slope of the
Andes in Chocó Department, Colombia, and west-

ern Ecuador. Species diversity of Dracontium is
highest in the Guianas (including the adjacent Ve-
nezuelan and Brazilian Amazonian regions), which
have seven species (D. amazonense, D. asperum. D.
dubium. D. guianense, D. nivosum, D. ргапсег. and
D. polvphyllum). A secondary center of diversity of
Dracontium is in Amazonian Peru (Loreto), where
five species (D. amazonense, D. angustispathum. D.
asperispathum, D. peruvianum, and D. spruceanum)
coexist.

Eight of the 23 South American species herein
of Dracontium appear as narrow endemics, often
known only from a few localities (D. bogneri, D.

602

Annals of the
Missouri Botanical Garden

dubium, D. guianense, D. longipes, D. nivosum, D.
polyphyllum, D. prancei, and D. ulei). Some of these
relatively narrowly ranging species are slightly
more widespread, such as D. amazonense, which
ranges from Amazonian Peru to Amazonian Brazil.
Only one species, D. asperum, occurs in the Do-
minican Republic and Puerto Rico; it is also found
in the Guianas and the islands of Trinidad and To-
bago. In South America, Brazil has the largest con-
tingent of Dracontium species, with 11 plus 2 ad-
ditional species likely to occur there (D. guianense

—

and D. plowmanii).

Species of Dracontium typically occur from near
sea level to about 500 m. West Andean D. croatii
is an Ecuadorian endemic species and is known
only from higher elevations, from 800 to 1200 m.
A few species may range from quite low elevations
to high elevations. These include D. pittieri (30—
1000 m). D. grandispathum (250-1200 т). and D.
spruceanum (25-1215 m).

Habitats.
itats from Premontane moist forest (P-mf), Tropical

Species of Dracontium occur in hab-

moist forest (T-mf), Premontane wet forest (P-wf).
and Tropical wet forest (T-wf). Most of the species
occur only in one life zone: D. amazonense, D. du-
bium, D. guianense, D. margaretae, D. prancei, and
D. ulei in Tropical moist forest (V-mf); D. gigas and
D. grayumianum in Tropical wet forest (V-wf). Some
species occur in two life zones (D. angustispathum,
D. asperispathum, D. bogneri, D. croatii, D. gigas,
D. grandispathum, D. longipes, D. nivosum, D. pit-
пегі, D. plowmanii, D. polyphyllum, and D. pur-
dieanum). Dracontium asperum, D. peruvianum, D.
soconuscum, and D. spruceanum are the only eco-
logically widespread species, all having been col-
lected in three different life zones.

Dracontium plants tend to occur along forest
margins and in somewhat disturbed or wasted areas
that are usually seasonally wet. Only one species,
growing in seasonal

D. margaretae, is found

swamps.

REPRODUCTIVE BIOLOGY
PHENOLOGY AND POLLINATION

Inflorescences in Dracontium are often produced
before new leaf production (D. soconuscum). They
may sometimes appear simultaneously with new
leaf production as in D. croatii, D. pittieri, and D.
spruceanum. Some species produce inflorescences
throughout the year (D. spruceanum), while others
bloom in the wet season (D. grayumianum and D.
pittieri) or in the dry season (D. gigas). These in-
florescences usually last four to six weeks, then the
spadix elongates into an infructescence if pollinat-

ed. The berries usually mature in a few to several
months, with 9 to 11 months noted in D. asperum
(J. Boos, pers. comm.).

The flowers of Dracontium are protogynous and
mature basipetally (Poisson & Barabé, 1998). For
a single flower, the ovary is anthesal usually one to
two weeks prior to anther dehiscence. It often takes
two to four weeks for all the flowers on a single
spadix to reach anthesis. The appearance of the
stigmatic fluid signals the receptive maturity of the
vary, often before the anthers of the same flower
have dehisced. The disappearance of the stigmatic
fluid signals that the stigma is no longer receptive.
The anthers of mature stamens dehisce along an
apical slit to form more or less rounded apertures.
The pollen exits in cohesive strands that contract
the stigma and its associated style (Fig. 26). The
pollen may be carried away by pollinators or may
fall naturally when dry onto a receptive stigma at
a lower position on the same spadix. Flowers at the
apex of the spadix must have pollen from other
plants in order to be pollinated.

This protogyny in Dracontium (common through-

—

out the family) serves to insure cross pollination,
Hand pollination for D. asperum was reported 1
cultivation by Hans Boos in Trinidad, West Indies.
In this case the inflorescence produced. berries
when cross pollinated and withered when there was
no pollen from another inflorescence available (J.
Boos, pers. comm.). When cultivated in the Mis-
souri Botanical Garden greenhouse, D. polyphyllum
developed voung berries with only one inflores-
cence blooming. However, no berries ripened be-
fore the infructescence rotted away. Two other spe-
cies, D. amazoense and D. prancei, have been hand
pollinated by the senior author in the Missouri Bo-
tanical Garden research greenhouse; both plants
failed to form berries. Another attempt at hand pol-
lination between these two species also failed. Fu-
ture reproductive studies are certainly needed in
the genus.

At anthesis, the spathe of Dracontium emits a
foul odor reminiscent of rotting meat, dead fish, or
decomposed vegetables. The timing and duration of
scent emission differ among species. Some species
release their scent from early in the morning until
late in the afternoon (D. gigas and D. polyphyllum),
others from late in the morning until early in the
afternoon (D. soconuscum), while others emit scent
from afternoon to late evening (D. croatii) for ap-
proximately a six-hour period (Guanghua Zhu, pers.
obs.). When the spathe is removed from the inflo-
rescence, the scent vanishes, indicating that the
scent is produced by the spathe instead of the spa-
Under SEM,

dix, as is commonly believed. there

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

are many structures associated with stomata on the

—

inner spathe surface, sometimes also on its outer

surface. These structures may be osmophores re-
sponsible for the emission of scent. The stomata
may be found opened or closed.

The pollinators of Dracontium remain unknown.
Croat (1975) suggested that Dracontium has a typ-
ical fly-pollination syndrome because of the trap-
like nature of the spathe of some species and the
foul scent the plants emit during anthesis, which is
typical of other fly-pollinated species in the Ara-
ceae. Houseflies and some fruit flies were observed
however,

to visit the flowers in the greenhouse:

these were also the only insects present in the
greenhouse. Flies and beetles were reported as vis-
itors of D. gigas when it was blooming at La Selva.
Costa Rica (M. Grayum, pers comm.). Large me-
tallic blowflies are reported to have visited D. as-
Boos,

perum in Trinidad as well as in Florida (J.

pers. comm.).

REPRODUCTION AND DISPERSAL,

Vegetative reproduction is by tubercles produced
at the apex of the tuber or via the production of a
tumor-like structure, which is part of the tuber
body. Tubercles are the most important means of
vegetative reproduction in Dracontium: they typi-
cally remain dormant for several years. Tests con-
ducted in North Carolina have shown that they may
remain dormant for two years despite different
treatments, with
growth hormones, use of different soils and different

including wounding, treatment
temperatures (P. Schmidt, pers. comm.). However,
disturbed tubercles may sometimes enlarge and
produce a leaf. Concomitantly, the principal tuber
usually rots away and is replaced by several smaller
plants originating from these tubercles. Sometimes
the smaller plants from tubercles may grow simul-
taneously while still attached to the parent for sev-
eral seasons before detaching from the principal
tuber.

All species of Dracontium are known to produce
berries and seeds in the wild. However, there is a
tradeoff between vegetative and sexual reproduc-
tion. When a plant regularly produces inflorescen-
ces and leaves (often alternately), its tubercles gen-
erally remain. dormant. A disturbance to the
principal tuber often causes its tubercles to enlarge
and to produce a plantlet; the principal tuber ceas-
es inflorescence production and instead produces
only leaves.

Populations show high sociability with remark-
able densities exhibited by D. gigas and D. gra-

yumianum. Individual clusters with many small

plantlets can be found within a few meters from the
parent plant. This suggests that short-distance dis-
persal via tubercules occurs in these species. Croat
(pers. comm.) suggested that Dracontium tubers
may be harvested by wild pigs because of their
starch content. At La Selva, a clump of D. gigas
was found near an agouti nest. The agouti’s digging
may have been responsible for the short-distance
dispersal of this species. However, there was no
The

tubercles of Dracontium easily detach from the par-

evidence that this animal was eating the tuber.

ent tuber when it is harvested or disturbed. Due to
their small size, the tubercles can be transported
easily in dirt when dug up. This theory is not in
conflict with the fact that many plants of Dracon-
пит are found as single individuals before reach-
ing the stage of sexual reproduction. As stated ear-
lier, tubercles remain dormant if the plant is not
disturbed, and the long-distance dispersal of seeds
by birds and mammals may result in an individual
plant growing in а new location away from the
mother plant. Long-distance dispersal of Dracon-
tium seeds is still unstudied, but the genus has a
typical bird-dispersal syndrome with colorful but
non-aromatic fruits and. seed, which can be indi-
vidually pecked out of an infructescence. However,
some Dracontium berries, e.g., those of D. grayu-
mianum, have a pleasant fruity scent and sweet
taste, which is typical of a mammal-dispersed seed
syndrome.

Uses

The ethnobotanical uses of Dracontium were
summarized by Plowman (1969) and later by Croat

994). Many Dracontium species are utilized by

—
—

indigenous people, including those of Hispanic cul-
ture, as having edible parts and possessing medic-
inal uses. One of the most common medicinal uses
of these plants is in the treatment of snakebite, doc-
umented for D. asperum, D. grayumianum, D. pit-
and D.

method of aroid medicinal usage varies in different

пегі, D. polyphyllum, spruceanum. The
areas. Roots and petioles of D. asperum are crushed
with sugar and alcohol yielding a tincture, which is
consumed at regular intervals for snakebite in Bra-
zil (Plowman, 1969). The remaining pulp is applied
to the area of snakebite by the same people (Croat,

1994).

and applied externally as a remedy for the poison-

Leaf infusions of D. pittieri were ingested

ous bite of the bocaraca snake (Bothreichis schle-
gelii Berthold) by indigenous peoples of Puntar-
enas, Costa Rica (Pittier, 1957). The Bribri Indians
of Costa Rica first boil an infusion of D. pittieri or

Annals of the
Missouri Botanical Garden

D. soconuscum leaves, then apply this to snakebite
wounds after cooling (Ginzbarg. 1977).
Dracontium spruceanum has been used exten-
sively by indigenous peoples. Pulp from scraped
tubers or split petioles of this plant is used by the
Mayna Indians of Peru and applied directly to
wounds (Croat, 1994). The scraped tuber and un-
heated inflorescences (or infructescence) are used
by the Achuar Indians of Peru to massage snake-
bite, while the pulp of the scraped tuber is also
applied to boils (Croat, 1994). The Achuar also use
the crushed tuber of this plant mixed with equal
parts of two Solanum (Solanaceae) species (“untu-
kar”

make tumors recede (Croat,

alleviate boils and to
1994). Tubers of D.
spruceanum are also cooked and eaten to relieve

and “syukahuito”) to

chest pain in Peru (Croat, 1994). Steward and Me-
traux (1948) reported that leaves of D. spruceanum
(as D. longipes Engl.) were rubbed on snakebite
wounds by the Amahuaca Indians of Ecuador.
Schultes and Raffauf (1990) reported that plants of
D. longipes Engl. were cultivated by the Kofán In-
dians of Colombia and Ecuador and used in a de-
coction for treating diarrhea. They further reported
that in Peru, tubers of these plants are ground into
a paste, wrapped in Calathea (Marantaceae) leaves,
warmed in a fire, and applied to snakebite.

Other medicinal uses have been reported for
Dracontium. The powdered tuber of D. asperum has
been used to treat the effects of asthma, anemia,
1892;
е Cointe, 1934). Juice from the tubers of this spe-

amenorrhea, and whooping cough (Peckolt,

cies is used to kill maggots in animals (Plowman,
1969). In Trinidad, D. asperum tubers have been
harvested as a substitute for potatoes after a period
1993).

of D. grayumianum are ground with water and used

of drying in storage (Boos & Boos, Tubers
1 Panama for treating hemor-
1994).
sion of the leaves of D. pittieri is used to kill mag-

by Chocó Indians i
rhaging during childbirth (Croat, An infu-
1957). In addition to being
1969). D.
polyphyllum is used as a remedy for hemorrhoids
(Croat,
spiders and stingrays (Levi-Strauss, 1952). The tu-

gots on wounds (Pittier,
used as a snakebite remedy (Plowman,

1994) and as an antidote for the venom of
bers of D. longipes are ground and used as a paste

1969).
Tubers of some species of Dracontium, such as D.

applied to snakebites Brazil (Plowman,
soconuscum and D. asperum, are edible. They may
be boiled and served like a potato or ground with
water and consumed as a juice (Croat, 1994).
Some species of Dracontium have horticultural
value and are favored by tropical gardeners and
aroid nurseries because of the snakelike patterning
of their petioles and the umbrella-like cut leaf

blades. Most are easy to grow and can be vegeta-
tively propagated by their tubercles. Several spe-
cies were described from cultivated plants, includ-
ing D. polyphyllum, D. asperum, D. croatii, and D.
gigas. Dracontium gigas has been well known and
commonly cultivated in European gardens since its
1869. Since then,
species has been repeatedly described and illus-

discovery in Nicaragua in this
trated in gardening publications and featured

plant exhibits (Seemann, 1869; Hooker, 1873; Mas-
ters, 1873; Watson, 1901; Macmillan, 1956). Other
species, including D. amazonense, D. prancet, D.

—

soconuscum, and D. spruceanum, are in cultivation
in botanical gardens in Germany, the Netherlands,
the United Kingdom, and the United States, as well
as in private nurseries in Florida. The market for
these plants is growing with increasing knowledge
of the genus.

RELATIONSHIPS

Several general trends can be observed from our
study of Dracontium, as well as from unpublished
analysis of 58 different character states. Some spe-
cies pairs share much in common. These include:
(1) Dracontium amazonense and D. prancet; (2) D.
grayumianum and D. soconuscum; (3) D. dubium
and D. purdieanum:; (А) D. gigas and D. pittieri; (5)
D. angustispathum and D. guianense; and (6) D.
asperispathum and D. spruceanum. In addition,
Dracontium margaretae is clearly related to D.
amazonense and to D. prancei. Dracontium gran-
dispathum is most closely related to D. asperispa-
thum and D. spruceanum. Dracontium grayumian-
um and D. soconuscum are often grouped together
with D. dubium and D. purdieanum. Our studies
indicate no infrageneric groups in the genus, but
two major clades are suggested. Morphologically,
these two clades can be distinguished by their pe-

duncles. All species with subterranean peduncles

~

г with peduncles only a few centimeters above
ground level group one clade (short-peduncle
clade), while those with a peduncle more than 30
cm long above ground level, with only one excep-
tion, group in the other clade (long-peduncle
clade). Our preliminary investigation also suggested
an evolutionary trend from long peduncles to short
(usually subterranean) peduncles within Dracon-
tium. The most basal members of the genus are D.
angustispathum and D. guianense, while the most
advanced members are D. amazonense and D. pran-
cei. The member with the most distinctive leaf
blade of the genus, D. margaretae, is also among
the advanced. group.

Volume 91, Number 4 Zhu & Croat 605
2004 Revision of Dracontium
TAXONOMIC TREATMENT the innermost the strongest; terminal segments 8—

967, 1753. TYPE: Dra-
contium polyphyllum L. (lectotype, designated
by Britton € Wilson (Scientific
Puerto Rico and the Virgin Islands, 5(1):

Dracontium L., Sp. Pl.

Survey of

1923)).
TAS Raf.. Fl. Tellur. 2. 1836 [1838]. TYPE: Eu-
ereia nigricans Raf.
Schott, Oesterr . Wochenbl. 1857.
^E

: ipic lontani : Schott
DURS 59 ‘hott. Oesterr. Bot. Wochenbl.
TYP N Sb ana x ‘hott.
Chersydrium Schott, t. Z. 15: 72. 1865.
drium jararaoa Schot
Godwinia See m., J. Bot. 7 re ‚ 96, 97.
Godwinia gigas бе,

—
—

TYPE:

eslerr.

—
=
PS

1869. TYPE:

Terrestrial, tuberous, perennial herbs, 1-5 m tall,
with | leaf (rarely 2) and with 1 (or rarely 2) inflo-
rescences, arising from an underground tuber bur-
ied 5-75 em deep: tuber + hemispheric, 2-20 em
diam., 2-10 em thick: with

convex below

flat above. few to
many tubercles among many roots:
smooth or strongly wrinkled, without tubercles and
roots; tubercles elongate, ovoid to ellipsoid or ey-
lindrical and often laterally compressed, 0.5-3 X
0.5-1 em, light brown; cataphylls 3 to 5. the in-
nermost the longest, 2-20 cm long above ground,
partially covering the petiole base, white-tinged
pink light brown (especially near the apex).
Leaves solitary or sometimes more, arising termi-
nally from tuber apical bud, tripartite: petioles 1—5
m long, 2-8 em diam. at base, 1-3.5 em diam. at

apex, light to dark or brownish green, sometimes

tinged brown near the base, mottled and streaked
with whitish or pale green areas forming a reptilian
pattern; armament varying from a smooth surface
to having heavy protuberances, sometimes with hor-
izontal elongate irregular projections bordering 2
differently colored areas, sometimes with spiny pro-
jections to 2 mm long; lower half of the petiole with
more eee es or projections, smoother above:
blades with 3 major divisions, each 0.5-1.5 cm
long. papyraceous to thinly coriaceous; upper sur-
face green, glossy or less glossy, rarely matte: lower
surface semiglossy or matte; sometimes with fen-
estrations along rachises or major veins: middle di-
vision sub-dichotomously divided into 3 sections:
lateral divisions sub-dichotomously divided into 2
sections; each section may comprise a single leaf
segment or be subdivided into 2 or 3 smaller sub-
sections accordingly; midrib and major veins con-
vex and light green on upper surface and conspic-
uously round-raised and paler on lower surface;
secondary veins + parallel and arching apically,
forming 2 collecting veins along the margins, with

0 X 3-7 cm,
fluent at base, often strongly decurrent downward

lanceolate to irregular, free or con-
along rachises, apically ac mar or caudate grad-
ually into 1, 2, or
yblanceolate or

3 apices; smaller leaflets

1-15
caudate, acute or rounded at apex, free at base, or

rarely :

+ triangular, —6.5 cm,

~

~

lecurrent downward partly covering the rachises,
or confluent completely at base with rachises com-
pletely covered by leaf tissue: irregular or often
pinnately arranged on the rachises; rachises mot-
tled similar to petiole in a much paler shade or
uniformly light green, sometimes tinged brown.
smooth or armed as petiole; length from petiole
apex to the first terminal subdivision of the middle
division as long as or to twice as long as lateral
divisions. Inflorescence solitary (rarely 2) arising
from apex of tuber before or after leaf development;
bracteoles З to 5, white-tinged pink to dark brown,
acuminate contracting to an apiculate apex; the
longest one (the innermost) completely covering the
underground part and the base of the peduncle,
sometimes longer than the peduncle and partly cov-
ering the spathe: peduncle reaching to slightly sur-
mounting ground level, to 2.5 m long. often shorter

than petiole, rarely exceeding petiole, 0.5-6 cm

diam., much like the petiole in appearance when
not covered by cataphylls, but tending to be

smoother; coloration. similar to that of petiole,
sometimes more rose or brown: spathe marcescent,
degrading on developed infructescence, narrowly
ovate to naviculiform, convolute at base, open
above, often hooded to broadly open: margins not
overlapping or overlapping at the base and forming
a tube, to broadly overlapping with only a small
apical opening: + acuminate at apex, erect to
а arching (less than 45°) to strongly arching
(45°-90°), externally violet-purple. often tinged
green or greenish, with obvious raphide cells, often
raised, sometimes with surface somewhat bullate,
internally reddish purple to maroon, glossy to se-
miglossy, sometimes with thin dry scales, often with
stomata surrounded by whitish or brownish spotted
glands, often with a whitish translucent area 0.5—
10 cm high around the base of the spadix, peri-
odically emitting at anthesis a foul scent like de-
composing vegetables or meat; spadix at anthesis
greenish to purple, cylindric (sometimes thinner at
apex), sessile or stipitate with a stipe 0.5-2.5 cm
long: spadix of infructescence 4-25 X 4-10 cm,
often 4 to 15 times longer and 4 to 8 times wider
than at anthesis. Flowers perfect, perigoniate, and
spirally arranged on spadix, opening basipetally:
tepals 4 to 6(8), green to purple, completely cov-
anthesis. Stamens (4)5 to

anthers before

ering

606

Annals of the

Missouri Botanical Garden

17(19); anthers yellow, open apically, turning red-
brown, sometimes with dark purple especially near
the opening after anthesis; filaments often slightly
dilated, subcompressed and abruptly contracted at
the apex into the connective; anthers exceeding
connective, linear-elliptic, yellow, turning reddish
brown, sometimes with dark purple, especially near
the aperture, after anthesis, dehiscing apically by
a vertical slit with rounded aperture at anthesis;

pollen emerging in strands; ovary of 2 to 5(7) loc-

4-lobed, covered with a clear sticky liquid at an-
thesis. Berries green when young, maturing to red-
dish, purplish, purplish red, purple-brown or or-
ange, covered with small whitish raphide cells,
sometimes with red dots (easily visible at 10X),
darkened apically, somewhat depressed around
style when persistent or rounded: seeds 1 to 7 pe
berry, variable in shape from round to reniform to
triangular to elongate, 0.5-1.0 em long. 0.4—1.2 em
wide, smooth or decorated dorsally with warty pro-
jections, usually with 1 to 3 dorsal ridges, these

continuous or interrupted, thin or thick. Chromo-

ules each with 1 ovule; style 2-5 mm long above
2n = 26 on all species counted to

tepals at anthesis, pale green to dark purple, per-
sistent in fruit or not; stigmas 2- or 3-, sometimes

some number:
date.

KEY TO THE NEOTROPICAL SPECIES OF DRACONTIUM
la. Blade segments linear, 1-1.5 cm wide, usually ascending at 45° angle from the petiole; growing in seasonal
swamps; Venezuela (Apure = Guárico), Brazil (Mato Grosso do ut) and Paraguay ———
e 13. D. margarerae рн
Ib lade segments not linear, 3-12 cm wide, spreading borisontelly tui asce nding at 45^ angle from ii et

when you eh growing in habitats other than seasonal swamps: southern Mexico to central Paragua
2a. Peduncle completely subterranean or not more than 10 cm Кеги 3 level; longest brac Su reach-
ing to base of or covering to % of the spathe
3a. Spathe c а Que not at an constricted; spadix lac king appendages at ape
4a. Spadix often concealed by spathe at anthesis; spathe margins broadly оо. at the
base for at least Y of the sp yathe.
5a. Spat 1e 28-35 cm long, 6-10 em wide at anthesis; endemic to Pará and Maranhão,

P 14. D. nivosum (le m.) G. Zhu
5b. Spathe to 20 cm long and 4.5 cm wide at anthesis: Brazil, Ve nezue MUR and Peru.
islucent scales.

D . amazonense G. Zhi & Croal
i more than 15 cm long, slightly arching toward apex (by up
to 45°); with a translucent area (at base of inner spathe surfac ii 0.5-1 em
high; known from Brazil (Amazonas and Roraima
19

3 Peru, Venezuela, and |

7b.
. D. prancei С. Zhu & Croat
Ob. Inner surface pf spathe semiglossy to velvety, obscured with translucent scales.
seeds reniform, laterally concave, with small cells along dorsal ridge: en-
dii mic to Goiás and s ent areas in Mato Grosso 5 Sul and Рага, Brazil
). bogneri G. Zhu & Croat
Seeds rounded, laterally convex, smooth along < а ridge: ranges fron
Acre, Brazil, to Pando, Bolivia . D. ulei K. А
›. Spadix visible from face view externally at anthesis; ; spathe | margins ETE to hardly over-
apping at the base; French Guiana, Suriname, Guyana, Brazil, and — Venezuela
polyphyllum L.
Spathe not cymbiform, constricted in lower V. to 34 and differentiated into a 2 Н and a
distal lamina: spadix often with one to several appendages (elongated and enlarged vadens al

b.

-

—

4

—
>

ine ме» e of Py never with translucent scales
10: 6 thin, strongly discontinuous diei to 1.5-2 mn
6. Colombia l

eeds with!
E rests, Darién, Panama, to Cho
10b. See a with 3 thick, continuous dene to 0.5
Mexico to central Panama
9b. Inner surfac e of spathe densely covered with transluc ent scales

1 high; tropical wet
>. Zhu & Croat

5 mm high; tropical moist
21. D. soconuscum Matuda

lla. Se E with 4 or 5 thin, slightly Mai ds Mul to 1.5 mm m high; ( suyana, Venezuela,
AAA . 8 7. D. d min Kunth

11b. See eds iid 3 continuous ridges to 0. 5 mm high; < Caribbean coast of Colombia, and
ela . D. purdieanum (Sc hott) Engl.

nezue
. Peduncle 30-2: 50: cm y 5 ground level; longest brac teole confined to base of peduncle, never reaching

the spa

12а.

ithe
Peduni le 30-90 em above ground level, less than half as long as petiole.

Volume 91, Number 4 Zhu & Croat 607
2004

Revision of Dracontium

1 За.

Spathe apex caudate, 3 to 5 times longer than the body of the spathe: berries apically
apiculate; endemic to Loreto and Napo, Peru . ar Tice IN G. Zhu & Croat
Spathe apex obtuse or acuminate, much shorter than the body of the spathe; berries truncate
to subtruncate apic cally; Central America, French Guiana, or South Fees 'a as far south as
gr d not in Peru.

14a. Spathe 58-78 em long. 13-21 em wide, obtuse at apex; seeds reddish pum 1-1.2

- bue with three dorsal ын Atlantic slopes of Nicaragua and Costa Rica —

- 8.

53 - ). gigas зыр Engl.
14b. Spathe 9—20 em long, 3-5 cm wide, acuminate at apex; seeds light brown, 0.5-0.7
em diam., with 1 dorsal ridge: Dominican Republic, Puerto Rico, Trinidad, Tobago,
Guyana, Surinam, French Guiana, Venezue ye нф Brazil
tl

l5a. Spathe 9-10 le acuminate at a slightly arching apically up to 45°
angle; seeds db convex, with many rds pits flanking on both sides of the
ridges: French Guiana, near Brazilian border |. 11. D. guianense G. Zhu & Croat
15b. Spathe 10-20 cm long, often arching apically by 45°—90° angle: seeds laterally
concave, with coarse, wart-like ки es flankin g the margins on both ow
of the ridges: ger Republic, Puerto Rico, Trinidad. Tobago, Guyana, 5
m. Venezuela, and Brazil 4. D. asperum K. Koch

rina
12b. I Peduncle 100-250 cm көйө ground leve ra usually more than half as long as petiole.

10a Spathe cymbiform, never differentiated into a proximal tube and distal lamina.
Sp athe obtuse at apex, widest in upper half.
8a. Seeds id ie dorsal ridges 4 or 5, strongly interrupted: spathe green ex-
уны, the margins broadly ove lapping: х Е hidden at anthesis; endemic to
the western slopes of the Andes in Ecuad 6. D. croatii G. Zhu
18b. Seeds reniform, dorsal ridge l, continuous; ac maroon externally, the margins
scarce d overlapping: spadix exposed at anthesis; endemic to the Pacific slopes
ta Rica 16. D. pittieri Engl.
17b. he acuminate at apex, widest in lower half.
19a. Spadix 23-35 cm long in fruit; petiole 2-6 m long; seeds pee d. with 3 strong.
continuous ridges to 2 mm high; Amazonian Peru and Brazil ——
——————— — 5. D. peruvianum G. Zhu & c roat
19b. S radi: 4-5 cm long in fruit: petiole 1-2 m long; Sedi reniform, with 3 weak
continuous ridges to 0.5 mm high: endemic to Acre, Brazil ———
uv ROTER Mum Engl.
lob. Vc usually not cymbiform, constricted near the base to yield a er ane and distal
lar
20. p 0.4—0.6 em diam., laterally convex, with 1 dorsal ridge: spathe usually wrinkled
or lobed along the margins; endemic to southern Peru —
——R Te Ds pm тапи G. Zhu & Croal
20b. Seeds 0. 7-1 em diam., laterally concave, with 3 ми к йын spathe er wrinkled
or lobed along the margins: С olombia, Ecuador, Peru, Brazil, de Surinas im.
21а. Inner surface of арай semiglossy or velvety, densely covered with translucent
cales; Colombia, Ecuador, and Peru К ра G. Zhu & Croat
21b. Inne surface of spathe semiglossy or ve Ivet ty, оаа rales
Spathe 45-50 cm long. 10-15 em wide, noy acuminate apically;
azonian Ecuador 00 .D.g randispathum G. Zhu y Croat
22b. Spathe 20-35 cm long, N em vide, E n acuminate apically; south-
ern Costa Rica to the Pacific slope of Colombia and Ecuador and in the
Amazon basin in ee сіс А olombia, xeb r, Peru, and выз il
(also in Surinam) 22. D. spruceanum (Schott) G. Zhu
1. Dracontium amazonense G. Zhu & Croat, Tuber hemispherical, 8-12 cm diam., 6-8 cm

sp. nov. TYPE:

de Picuruyacu,

Peru. Loreto: Iquitos, Altura thick, flat above, rounded and white to brown be-
near confluence of Río Nanay low, 10-20 cm below ground level; tubercles abun-

& Rio Amazonas, 3°40'S, 73°13'W, 28 Dec. dant, cylindrically elongated or rounded, 0.5-1 cm
1979, C. Davidson & J. Jones 9605 (holotype, diam., 0.8-2 ст long, borne around the periphery
MO: isotype, RSA!). Figures ЗА, 4. of tuber; roots whitish, 1-3 mm diam.; cataphylls 2

or 3, 5-22 cm long, 3-5 cm wide, pink-tinged or

Herba usque plus quam 2 m alta; petiolus 1.3-2 m light brown, reaching or surpassing ground level.

longus; pedunculus subterraneanus, 0-2 em longus; od
5

a 10-13 em longa, 3

Leaves solitary; petioles 1.3-2 m long above ground,
2.5—4 cm diam. at midpoint, dark green, contrast-

diam.; baccae globosae. 0.5-0.7 ст diam.; semina dole ingly mottled with dirty white or pale green blotch-

suffusa aurantiaca, usque 0.6 ст diam. es and forming a reptilian pattern, usually smooth

Annals of the
Missouri Botanical Garden

Figure 3. A-D, Flowers. —A. Dracontium amazonense (Croat 56898). ا‎ with p stigmas. —B.
polyphyllum (Croat 74210). Apex of spadix showing short styles and stamens. — . spruceanum (б. Zhu i4
Close-up of flower showing weakly HUNE stvle and a ring of stamens. —D. D. soconuscum (G. Zhu 1502). Spadix

ex

with a cluster of appendages at ¿

Volume 91, Number 4 Zhu & Croat 609
2004 Revision of Dracontium

0.5 cm

Figure 4. A-D, oo amazonense.—A. (Croat 56898). Spathe showing side view. —B. (Croat 71895). Spathe
showing front view. —C. 1 65898). Spathe with cut-away view showing spadix at anthesis. —D. (Davidse & Jones
9605). Reeds i in side En

610

Annals of the
Missouri Botanical Garden

in upper half and with irregular protuberances in
lower half; juvenile blades sagittate, or sagittately
lobed; mature blades spreading horizontally, 1—1.2
rarely fenestrate, never

m diam., subcoriaceous,

variegated, often without raphide cells or dark
markings, glossy and dark green above, semiglossy
and medium green below; middle division once or

4045

cm, with terminal subdivision consisting of three

twice trichotomously branched, 45-60

sections, with each basal subdivision consisting of
lateral divisions twice dichoto-
40-55 Х 40-50 cm,
minal subdivision consisting of 2 sections,

many segments;

mously branched, with ter-
with
basal subdivision consisting of many segments; ter-
minal and subterminal sections free, each consist-
ing of many segments; leaf segments often entire,
broadly oblanceolate, more than 5 cm wide on each
side of the major ribs, narrowly elliptic, at least
some of the basal segments free from each other,
often without contrastingly smaller rounded or tri-
angular segments; apices acuminate; ultimate seg-
ments 10-15 cm long, often confluent with penul-
timate segments; other segments 7-13 cm long;
penultimate segments free from subterminal sec-
tions; medial segments free from basal subdivi-
sions; basal segments present, free from each other;
rachises patterned similar to petiole but in much
paler shades, smooth; tertiary veins obscure above
and weakly raised below; bracteoles 1 or 2, 6-22 X
1-2.5 cm, pink tinged, the longest one longer than
the peduncle, 5 up to % of the spathe. In-
florescence solitary or two, appearing before new
leaf; peduncle 0-2 cm long above ground, 1-1.2 cm
diam. at midpoint, often almost completely subter-
ranean, scarcely mottled, whitish tinged pink,
smooth; spathe (6—)10—13 X 3-4.5 em, cymbiform,
cucullate, often arching 90°, apex acuminate; inner
surface velvety, violet-purple, with translucent area
obvious, 0.5-1.5 em high, shorter than spadix; out-
er surface maroon, tinged green, matte; margins en-
tire, slightly overlapping at the base; veins obscure
inside, conspicuously darker or paler than the
spathe, brown; spadix often hidden, sessile, cylin-
dric, narrower at apex, brownish purple, 2.5—4 X
0.8-1.2 cm at anthesis, never with appendages at
apex; flower tepals 4 to 5, 1.5-2 X 1-2 mm, light
brown or brownish purple; stamens 6 to 8; filaments
1-2 mm long; anthers 0.5 mm long, completely ex-
serted; ovary 3-locular, white; stigma unlobed, or
3-lobed; style 0.5-2 mm long above tepals, brown-
ish purple, persistent. /nfructescence with spadix
3.5 em long, 1.5 em diam. in fruit; berries 0.5—0.7
х 0.6 em, globose, apically rounded; young berries
pale green; mature berries with abundant raphide
0.5-0.6 cm diam., reniform, light

cells; seeds

brown, laterally depressed; dorsal ridges evident,
3, + continuous, more than 1 mm thick, warty
along both sides, appearing as strongly reduced lat-
eral ridges. Chromosome number 2n = 26 (С. Zhu
1454

Phenology. Flowering known only in March;
mature fruits known only in December.

Distribution and habitat. Drucontium amazo-
nense is known from Amazonian Venezuela (Bolf-
var), Brazil (Amazonas and Рага), and Peru (Lore-
to). It occurs in the Tropical moist forest (T-mf) life
zone, at elevations of 60 to 100 m.

Discussion. Dracontium amazonense is easily
confused with D. polyphyllum in both sterile and
ertile condition. Mature leaves of both species
closely resemble one another, and their inflores-
cences are superficially similar. However, D. ama-
zonense differs in its laterally concave seeds (vs.

aterally convex in D. polyphyllum) and the spathe
in D.
polyphyllum), as well as by its usually hidden spa-

usually arching 90° apically (vs. arching 45°

dix (vs. exposed in D. polyphyllum)

A tuber of the type collection (Davidson & Jones
9605) of D. amazonense was sent to the Missouri
i 1979. The plant
bloomed the following spring, and a fertile ion

nen (Croat s.n., MO 4369881) was prepared ir
Apri |

species were brought into cultivation at the Mis-

Botanical Garden December

1980. Two years later, two more tubers of dos

souri Botanical Garden from Manaus, Amazonas,
Brazil (Croat 53561, June 1982). However, when
we started to study the genus Dracontium 10 years
ater in 1992, both Davidson & Jones 9605 and
Croat 53561 were missing from the greenhouse. In-
stead, D. amazonense was represented by two other
numbers, Croat 56898 and Croat & Grayum 59844,
in the greenhouse, each with several mature plants.

These plants must have been mislabeled, since
both numbers apparently originated from Costa
Rica, where D. amazonense is unknown. Croat
56898 was collected by Helen Young from La Sel-
va, in the province of Heredia, where only D. gigas
occurs. Croat & Grayum 59844. was collected from
the Osa Peninsula, where only D. pittieri is known.
Therefore, the cultivated plants labeled as Croat
56898 and Croat & Grayum 59844 in the Missouri
Botanical Garden greenhouse probably originated
from the collections Davidson & Jones 9605 and
Croat 53561 and represent D. amazonense.
Dracontium amazonense is one of the most easily
grown species in the genus. It blooms regularly and
propagates easily in the greenhouse by means of
to the authors’ knowledge it

tubercles. However,

had never produced fruit by means of either self-

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

or cross-pollination. This species has been widely
distributed by the Missouri Botanical Garden, un-
der the number Croat 56898 and the name D. gi-
gas, to many institutions worldwide and private ar-
oid growers in the United States.

neo а Chacaras
JW of Manaus, J. Croat 53561,
56898 (MO); Tefé, Lago Tefé, NW shore. T. Plowman et
al. 12510 (MG, MO); mouth of Rio Bauana, J. Plowman
et al. 12550 (MG, MO, NY). Pará: Rio Juruá. Bom Fim.
Ule 5286 (MG). PERU. Loreto: Quebrada она e
aed bie pu Río 5 P. Ma 299
(U). EZUELA. Bolívar: Santa Elena de Taken. ean
мр сатров S 2 inicia Peña, Tamayo 3188 (F,
US, VEN).

Cultivated plants. Peru. Loreto: Altura de Pecuruyacu,
TYPE: Davidson & Jones 9605, (MO 4369881). cult. at
pie ч : Mera orae ) [represented by G. Zhu
1454, 460, 146 5 1465, 1489, 1514,
1516 B br pene Wenn s. T. B. Croat 53561
(МО), cult. at MBG. Ecuador. Napo: : Puyo, € . McDaniel

| В. Croat т (МО), cult. at MB(

BRAZIL.

Paratypes.

—

Zhu &

Mishuya-

N

Dracontium angustispathum G.
Croat, sp. nov. TYPE: Peru. Loreto:
cu, near Iquitos, LOO m, in forest, G. Alug 254
(holotype, US!; isotypes, F!, NY!). Figure 5.
Herba usque pra quam 2 m alta; petiolus 1-2 m lon-
gus; lamina 35-55 cm lor nga, 25-35 cm lata; pedunculus
15-65 cm longus, 0.5-1.5 em diam.; spatha 6-10 em lon-
.5-2 cm lata, i basi, apice 20-50 cm longa:

—

Sa
ga.
extus impolita, sordide purpurea; intus purpurea: ud Ix
2-5 cm longus, 0.5-1 em diam.; tepal run-
neola, 0.5-0.65 cm longus, 0.4—0.5 cm lata.

a 5-7; Зе mina

5—0 cm
thick. flat above, rounded and white to brown be-
low, 10—15
dant, rounded or cylindrically elongated, 0.5-1 cm
diam., 0.6-1 cm long, borne around the periphery
of tuber: cataphylls 2 or 3, 2-15 cm long. 1-2.5
light
ground level. Leaves solitary; petioles 1-2 m long

Tuber hemispherical, 6-10 cm diam..

> em below ground level; tubercles abun-

cm wide, brown, reaching or surpassing
above ground, 1.5-3.5 em diam. at midpoint, dark
green or brownish green, contrastingly mottled with
dirty white or pale green blotches and forming a
reptilian pattern, usually smooth in upper half and
with irregular protuberances in lower half: juvenile
blade sagittate, or sagittately lobed; mature blades
spreading horizontally, 1-1.2 m diam., thinly cori-
aceous, rarely fenestrate (sometimes fenestrate in
juvenile leaves), never variegated, without raphide
cells or dark markings, semiglossy and medium
green above, matte and medium green below; mid-
dle division once or twice trichotomously branched.

35-55 X 25

sisting of three sections, with each basal subdivi-

5-35 em, with terminal subdivision con-

sion often consisting of an entire segment; lateral

divisions twice dichotomously branched, 35-55 х
25-35 cm, with terminal subdivision often consist-
ing of an entire segment, with basal subdivision
often consisting of an entire segment; terminal and
subterminal sections free, each usually consisting
of a single segment; leaf segments often. entire,
broadly oblanceolate, more than 5 em wide on each
side of the major ribs, lanceolate, mostly free from
each other in each division, without contrastingly
smaller rounded or triangular segments; apices cau-
date: ultimate segments 20—35 cm long: basal seg-
ments absent; rachises patterned similar to petiole
but in much paler shades, smooth: tertiary veins
prominent above, or weakly raised below; bracteoles
2 or 3, 5-20 cm long, 1-2 em wide. dark brown or
light brown, the longest one much shorter than the
peduncle, confined at the base of the peduncle. /n-

Jlorescence solitary, appearing before or after new

leaf: peduncle (35—)45—65 cm long above ground,
0.5—1.5 em diam. at midpoint, less than half as long
as the petiole, mottled similar to petiole but deeper
in color, dark green, smooth in upper half; spathe
6—10 X 1.5-2 em, cymbiform, non-cucullate, erect
or slightly arching, apex caudate, 3 to 5 times long-
er than the remainder of the spathe; inner surface
semiglossy, maroon, with translucent area obscure
(to 3 mm height); outer surface dark purple, matte:
margins entire, broadly overlapping or convolute in
the lower two-thirds; veins obscure inside and out-
side, similar to the spathe in color; spadix hidden,
sessile, cylindric, light brown or purple, 2-5 cm
long. 0.5-1 em diam. at anthesis. Flower tepals 5

to 7. 1.5-2 X 1-1.5 mm, pale green; stamens 6 or
7: filaments 1.5-2 mm long; anthers 0.5-1 mm
long. slightly exserted; ovary bilocular, pale green:
stigma unlobed, or 2-lobed; style 1-2 mm long
above tepals, green, persistent. /nfructescence with
spadix 6—9 cm long, 1.5-2 cm diam. in fruit; berries

0.8-1 em thick, obliquely ob-

medium

.1-1.8 em diam.,

ovoid, apically apiculate; berry
green; mature berry orange, with abundant raphide
cells: seeds solitary, 0.5-0.65 X 0.4—0.5 cm, round-

ed or reniform, light brown, laterally flattened: dor-

young

sal ridges obscure.

Phenology. Flowering from July to April; ma-
ture fruits from August to April.

Distribution and habitat. | Dracontium angustis-
pathum is found in Loreto Department in Peru, and
there is also one collection from Vaupés in Colom-
bia. It occurs in Tropical moist forest. (T-mf) and
1 wet forest (T-wf) life zones (Holdridge et
‚ 1971), often in swampy areas, at elevations of
100 to 180 m.

Local names.

"Anakaho" (King 416, F):

“jer-

Annals of the
Missouri Botanical Garden

J, Dracontiurt angustispathum. —A. Cultivated plant by John Banta, originally collected in ru in
oto by Josef Bagnet, —B. Specimen showing inflorescence, portions of pe tiole, tuber (Plowman et al. 6720, GH).
wium specimen a close-up of infructescence (Stein 3999), —D. eeds showing dorsal view and

m view (bottom) (Vásquez z et al. 80€

gurt

. Herba

Volume 91, Number 4
004

Zhu & Croat 613

Revision of Dracontium

(Martin & Lau-Cam 1315,

gon sacha del bajo”

ECON

Discussion. Dracontium angustispathum does
not resemble any other member of the genus. It is

characterized by its thin spathe less than 2 em wide
at anthesis, with a caudate apex 3 to 5 times longer
than the body of the spathe (hence its epithet), leaf-
blade divisions usually consisting of a few (3 to 5)
segments; and usually l-seeded berries apiculate
apically. This species has been previously identi-
fied as the partially sympatric D. loretense |D. spru-
ceanum|, which has a much longer peduncle. Cul-
tivated plants of D. angustispathum are only known
from John Banta’s nursery in Florida.

The new species Dracontium angustispathum
was previously noted (as nomen nudum) to occur
in Peru (Vásquez et al., 2002 [2003 |).

Paratypes. COLOMBIA. Vaupés: Río Apaporis. al
mouth of Río Pacoa, Schultes 14799 (GH). PERU. Lor-
eto: May е on Rio Amptyacu, Plowman et al.

A

6720 (G m pe Ө ейде Esta. Exp. Inst. Inv. ПАР.
Quebrada Brashico. Vásquez et al. 16524 (MO): Almen-
dras, Vásquez & Jaramillo 4938 | MO), 7595 (MO): Iquitos
ci tu, Inchaustegut s.n. . Williams 3750 (V)

as. Pebas, Bora s community of Brillo Nuevo.
7 man et al. 6815 (GH). cy & Alcorn 198 (F); Río
Ampiyacu, Bora Puca 9 a Taa ae Hahn et
17 Stein 3999 (MO); Rio Nanay, Casería Mis-
W of Iquitos, Callicebus Biologic : We түе,
Foster 1389 (Е): Pinto-Cocha, Williams 82 ; Puerto
Almendras, Vásquez et al. 8081 (MO). Napo: "Río Napo.
Negro Urco, Martin & Lau-Cam 1315 (ECON): Río Santa

María, trail E of Secoya, village of “Vencedor,” King 416
ў iol., Vásquez et al. 6761 (MO): Río

—.
г]
>
me
—
2
@
=
;
Y
a

illip & Smith 29351 (NY. US): Rio

s чо. tributary of Río Putumayo, Bellavista Paujilillo.
vaire 1757 (MO).

i plants. Peru. Unknown чыга locality, J.

Bogner s.n. (M). cult. in Unie d States, Florida. Alva. John

anta’s Nursery, E. Spec Río ied collecte

by van der Werff, vouc 1 Nov. 1996, Croat 79128

; Lore E

3

Dracontium asperispathum G. Zhu & Croat,
T Pe Maynas. Pebas

71°49'W, 10 Apr.

sp. nov. : Peru. Loreto:

on Río Ampiyacu, 3°10'S

1977, T. Plowman, К. E. Schultes & O. Tovar
6729 (holotype, F-1825130': isotypes. F-
1823999!, GH!). Figure б.
Petiolus 1-2.5 m longus; lamina 50-65 cm pisi 50-
60 em lata: pedunculus 1-1.45 m longus, 1-2.5 em diam.:

spatha 28—46 ст longa, 4—6 cm lata, cucullata a extus
"ае sordide viridis; intus velutina, purpurea; a
.5-6 0.7—1 em diam.; tepala (4—)5—6(— 7):
semina iin 0.6—0.8 em diam.

1 longus,

uw

^
z

Tuber hemispherical, 5-15 cm diam., 4-8 cm

thick, flat or slightly sunken above, rounded and
white to brown below, 5-20 em below ground level.
0.8-1 cm diam., borne

Tubercles few. rounded,

around the periphery of tuber; roots 2.5-3 mm
diam.; cataphylls | to 3, 6-22 X 1.5-3 em, pinkish
or light brown, reaching or surpassing ground level.
Leaves solitary; petioles 1-2.5 m long. 2.54 cm
diam. at midpoint, dark green or medium green
tinged brown, contrastingly mottled with dirty white
or pale green blotches and forming a reptilian pat-
tern, smooth or sometimes with spiny projections:
juvenile blade sagittate, or sagittately lobed; mature
blades spreading horizontally, 1—1.4 m diam., sub-
coriaceous, sometimes fenestrate, never variegated,
without raphide cells or dark markings, semiglossy
and dark green above, matte and medium green
below: middle division twice trichotomously
branched, 50-65 X 50-00 cm. with terminal sub-
division consisting of three sections, with each bas-
al subdivision consisting of many segments; lateral
47—60 x
with terminal subdivision consisting of

divisions twice dichotomously branched,
15-55 cm,
two sections, with basal subdivision consisting of
many segments; terminal and subterminal sections
free, each usually consisting of a single segment or
each consisting of a few segments; broadly oblan-
ceolate, more than 5 em wide on each side of the
major ribs, ovate-oblong or elliptic or lanceolate,
mostly free from each other in each division, often
without contrastingly smaller rounded or triangular
segments; apices acuminate, or rarely acute: ulti-
mate segments 20-32 cm long, free from penulti-
mate segments; other segments 9-20 em long: pen-
ultimate segments free from subterminal sections;
medial segments often free from basal subdivisions:
basal segments present, free from each other: ra-
chises patterned distinct from petiole, pale green,
smooth: tertiary veins prominent above and weakly
raised below; bracteoles | to 4, 4-24 ст long. 1.5—
3 em wide, light brown, the longest one much short-
er than the peduncle, confined to the base. /nflo-
rescence solitary, appearing before or after new leaf:
de le (56-)100-145 cm long above ground, 1—
5 em diam. at midpoint, more than half as long
as the petiole or sometimes as long as or longer
than the petiole, mottled similar to petiole but
deeper in color, dark green, smooth in upper half
or with irregular protuberances in lower half «
spiny projections; spathe 28-46 cm long, 4—6 cm
wide, non-cymbiform, constricted at a certain point
and differentiated into a proximal tube and a distal
lamina (blade), erect or slightly arching, apex acu-
minate: 8-12 em long, 4-6 em wide at widest point;
lamina 3 to 5 times longer than the tube; inner
surface covered with dense, translucent scales 1—2
mm long, olive-brown or red-purple, with translu-
cent area obvious, 8-15 em high, 1.5-3 times long-
er than spadix: outer surface green or green tinged

614 Annals of the
Missouri Botanical Garden

Figure 6. A-D, Dracontium ni Mi iria (Plowman et al. 6729). —A. Herbarium type specimen. —B. Herbarium
type specimen showing inflorescenc ;. Herbarium type specimen showing infructescence. —D. Seeds in side view.

Volume 91, Number 4

Zhu & Croat
Revision of Dracontium

brown, matte; margins entire, broadly overlapping
at the base; veins obscure inside and raised out-
side, similar to the spathe in color; spadix hidden,
stipitate, cylindric, brown or purple or dark purple,
3.56 X 0.7—1 cm at anthesis, never with append-
ages at apex; stipe 0.5-1 X 0.5-0.8 cm at anthesis,
light brown; flower tepals (4)5 or 6(7), 0.5-2.5 X
—2 mm, purple or dark purple; stamens 5 to 7
filaments 0.3-2 mm long; anthers 0.3-0.5 mm long.
hidden or slightly exserted; ovary 3-locular, pale
green or white; stigma unlobed; style 0.5—1.5 mm
long above tepals, purple or green, persistent. /n-
fructescence with spadix 8-16 X 2—4 cm in fruit:
berries 0.7—0.8 0.7—1 сї 2-seeded,
obliquely obovoid, apically rounded or subtruncate:
young berries medium green; mature berry orange.
without reddish dots and raphide cells; seeds 0.6—
9 cm diam., reddish brown, laterally
flattened; dorsal ridges obvious, 3, often strongly
interrupted, with the central ridge contrastingly
raised, more than 1 mm thick, 0.1—0.2 mm high.

warty along ridges.

—

n, I- or

rounded,

Phenology. Flowering from January to Septem-
ber; mature fruits from April to August.

Distribution and habitat. Dracontium asperis-
pathum ranges from the Amacayacu area in Colom-
bia (Amazonas) to Amazonian Ecuador (Napo) and
along Río Amazonas and Río Маро in Peru (Loreto).
It occurs in Tropical moist forest (T-mf) and Pre-
montane moist forest (P-mf) life zones (Holdridge et
al., 1971), at elevations of 100 to 230 m.

Local name. "Jergón sacha” (Williams 1942, F;
Plowman & Martin 1661, ECON

Discussion. Dracontium asperispathum is easily
confused with D. spruceanum where their ranges
overlap in the upper Amazon basin because they
have very similar leaves and a long-pedune ulate
elongated purplish spathe, but the former differs in
having the spathe inner surface covered with dense,
translucent scales (hence, the name asperispathum).

The new species Dracontium asperispathum was
previously noted (as nomen nudum) to occur in

2002 [2003]).

Peru (Vásquez et al.,
COLOMBIA. Amazonas: Amacayacu,
Par. Nac. Nat. Amacayacu, Trocha de hpi J. Pipoly
15612 (MO). ECU ADOR. Napo: Pa Yasuní, Pozo
Petrolero Conoco-Amo 2, D. Neill et al 8160 (С М, MO,

C PERU. Loreto: Explorama, Napo Camp, Las
Amazonas, Quebrada Suc usari, ent et al. 42629

Paratypes.

: е
Explorama Сатр, Rfo Amazonas above toot of Río
Napo, Gentry et al. 29076 (MO); Iquitos, Maare 189
(ECON); Picurugacu, Plowman & Martin 1661 (ECON);
Río Ampiyacu at Pebas, Plowman et al. 6728 (F, GH);
Río Amazonas at Pebas, Williams 1750, 1942 (F); Río

—

Amazonas, Caballo-Cocha, Williams 2119 (F, US); Río
Napo, Isla Inayuga, Croat 20550 (F, MO); Río Yaguasyacu,
Brillo Nuevo, Plowman et al. 6820 (GH); Ushpacafio, near
Iquitos, Tina & Tello 2054 (ECON): Varadero de Mazan
from Río Amazonas to Río Napo, Croat 19391 (MO): Hío
Williams 155 (F).

—

Пауа,

4. Dracontium asperum К. Koch, Wochenschr.
33: 259. 1859. TYPE: Surinam. Nickerie, 12
km N of Lucie River, 3 km S of Juliana Top,
3736'—41' М, 56730'—34" W, 300 m. H. S. Irwin
et al. 55045 (neotype, designated by Zhu &
Grayum (1995: 522), NY!; isotypes, COL!, F!,

GH!, K!, US!, VEN!). Figure 7.

Dracontium elatum Masters, Gard. Chron. 1: figs. 58, 344.

370. TY Guyana. Distributed by [, inde n ind i in

rss nursery, Sanders 1920 (lec
tolype, , K).

Dracontium foecundum fook. f.. Bot. Mag. 1885: t. 6808.
1885. n Guyana. d Corentyne River,
near coast, 2 Mar. 1882, W. W. E.
Im Thurn s.n. [from E TR (holotype. K!).

flat or

4-16 X 3-8 cm,

whitish to

Tuber hemispherical,
slightly convex above,
brownish below, 15-35 em below ground level: tu-
bercles abundant, cylindrically elongated, 0.5-1 X
1-3 ст, borne around the periphery of tuber; roots
white, 2-3 mm diam.; cataphylls | to 3, 14-35 X
2-5.5 em, pinkish or light brown, reaching or sur-
passing ground level. Leaves solitary or sometimes
2 or more per tuber; petioles 1-2 m long above
at midpoint, gray or whitish

rounded and

ground, 2—4 ст diam.
green (especially when young) or medium-green-
tinged brown, scarcely mottled, usually smooth in
upper half and with irregular protuberances in low-
er half; juvenile blade sagittate, or sagittately lobed;
mature blades ascending to to the petiole
spreading horizontally, 1-1.3 m diam.,
ceous, rarely fenestrate, never variegated, without
raphide cells or dark markings, glossy and medium
green above, glossy and dark green below; middle
division twice trichotomously branched, 1-1.2 cm
long, 0.9-1.1 cm wide, with terminal subdivision
consisting of three sections, with each basal sub-
division consisting of many segments; lateral divi-
sions 3 times or more dichotomously branched,
0.75-0.98 х 0.8-1 cm, with terminal subdivision
consisting of 2 sections, with basal subdivision con-

papyra-

sisting of many segments; terminal and subterminal
sections free, each consisting of many segments:
leaf segments bilobed or irregularly lobed, broadly
oblanceolate, more than 5 cm wide on each side of
the major ribs, ovate or oblanceolate, at least some
of the basal segments free from each other, often
with contrastingly smaller rounded or triangular
segments alternating with larger segments; apices

616 Annals of the
Missouri Botanical Garden

*

+ >
Figure 7. A-D, Dracontium asperum. A, В. Photos taken at Orange Grove Estate, Trinidad, by Hans Boos.
нне scence " anthesis, —B. Inflorescence i one side removed to expose interior of spathe and the spadix al
nthesis. —C. (C. Zhu 1509). Cultivated plant by Hans Boos in Trinidad showing base of petiole and infructescence

with i immature е and persistent spathe. | Photo. hy Hans Boos. —D. Seeds from Trinidad sent by Julius Boos.

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

acuminate, or acute (rarely); ultimate segments 12—
20 cm long, free from penultimate segments: other
segments 6—15 cm long: penultimate segments not
free from subterminal sections; medial segments
confluent with the basal subdivisions; basal seg-
ments present, free from each other; rachises pat-
terned similar to petiole but in much paler shades.
with spiny projections (sometimes); tertiary veins
conspicuous above and weakly raised below: brac-
teoles | or 2. 4.5-37 X 1.5-3 em, dark brown mot-
tled with light brown, the longest one much shorter
than the peduncle, confined at the base. /nflores-
cence usually solitary, rarely 2, appearing before
new leaf; peduncle 5-17 cm long above ground.
0.5-0.8 cm diam. at midpoint, less than half as long
as the petiole, mottled similar to petiole but deeper
in. color. brown-green, often with irregular protu-
berances: spathe (10)13—20 X 3-5 cm, cymbiform.
cucullate, often arching 4577907, apex acuminate:
inner surface velvety, maroon or purple-red or red-
purple. with the translucent area obvious, 1-2 ст
high. shorter than spadix; outer surface maroon,
tinged green or dark purple, matte; margins entire,

hardly overlapping at the base; veins obscure. or
obvious inside and outside, similar to the spathe in
color, marcescent on developing infructescence:
spadix exposed, sessile, cylindric, purple. 2.6—4 х
0.8—1.1 cm at anthesis, never with appendages at
apex: flower tepals (4 to)5 or 6(to 7), 3—4 mm long.
1-2 mm wide, dark purple: stamens (5)6 or 7: fil-
34.5
completely exserted; ovary 3- or
3-lobed:
above tepals, dark purple, persistent. /nfructescence
with spadix 8-15 X 3-4 cm in fruit: berries 0.8—
1.2 cm diam., 0.8-1 em thick, subglobose. 3- to 6-
angular, light
green; mature berry purplish brown, with abundant

aments mm long: anthers 1—1.5 mm long.

1-locular. pale

green; stigma 2- style 1-3 mm long

apically subtruncate; young berry
reddish dots and raphide cells (dried berries); seeds
l- to 3-seeded, 0.5—0.7 cm diam., triangular (+) or
aterally depressed; dorsal

rounded, light brown,
ridges obvious, 3, continuous, more than 1 mm
thick, warty along both sides, these appearing as
another set of strongly reduced lateral ridges. Chro-
mosome number 2n = 26 (Bogner 1132, M; Peter-
sen, 1989).

Phenology. Flowering mainly from January to
March, also in December and from June to August:
mature fruits from January to August

Distribution and habitat. Dracontium asperum
is a widely distributed species in the Guyana high-
lands from coastal Surinam and adjacent Brazil
(Amazonas), throughout Guyana, ranging into the
West Indies from the islands of Trinidad, Puerto

Rico, and Dominican Republic. It is likely to be
found in northeastern Venezuela since it is phyto-
geographically related to Trinidad. It occurs in the
Tropical moist forest (T-mf) life zone (Holdridge et
al., 1971), at elevations of 30 to 330 m. Dracontium
asperum is also known from Dominica and Marti-
(Jo Ann Baptiste & Julius Boos,

comm.). Julius Boos (pers. comm.) suggests that

nique pers.
some of the distribution of this species in the West
Indies is partly the result of its probable distribu-
tion by means of its use as a journey food by native
peoples moving from island to island.

Discussion. Dracontium asperum is distin-
guished by its often strongly hooded spathe with
the margins broadly overlapping in the lower half
at anthesis, hidden spadix, peduncle much longer
than the longest bracteole 10-35 ст long above
ground level, laterally concave seeds with a single
strongly interrupted dorsal ridge coarsely orna-
mented with wart-like structures flanking the ridge.
and usually many tubercles at the tuber apex. One
of the most perplexing taxonomic problems in the
genus Dracontium was the confusion involving D.
asperum and D. polyphyllum, resolved by the des-
ignation of a neotype for the former and an epitype
for the latter (Zhu & Grayum,
asperum is also similar to D. prancei, which differs

1995). Dracontium
having the bracteoles usually longer than the
peduncles and covering the base of the spathe.
Dracontium Koch
(1859) over a century after D. polyphyllum (1753).
from a plant introduced from Surinam and culti-
vated at the Berlin Botanical Garden that had been
obtained from the Botanical Garden in Amsterdam.

asperum was described by

The holotype of D. asperum prepared by Koch and
presumably deposited at B was either destroyed or
"sl.

Dracontium polyphyllum differs from D. asperum
slightly broader (6-12.5 cm

~

in having a shorter,
long, 3—5 em wide), slightly arching spathe (arching
24

overlapping at base at anthesis. The inner surface

5° angle) with the margins hardly or slightly

is violet-purple with a whitish area 0.5 em high
around the spadix at the base. The peduncle is 0—
5 em long above ground level, and the cataphyll is
often longer than the peduncle and surpassing the
base of the spathe. Berries have 3 seeds that are
0.4—0.7 cm in diameter, convex on both sides with
a continuous dorsal ridge. In addition. the tuber
usually has only a few tubercles at the apex. The
species is known from northern Brazil, French Gui-
ana, and Surinam. In contrast, D. asperum differs
from D. polyphyllum in having a spathe 13-20 cm
4.5°—90°

apex and which is strongly hooded with the margins

long, 3-5 em wide, often arching al the

Annals of the
Missouri Botanical Garden

broadly overlapping in the lower half at anthesis,
often completely covering the spadix. The inner
surface is purple to purplish red with a whitish area
1-2 cm high at base. The peduncle is 14—45 cm
long above the ground and the cataphyll is much
shorter than the peduncle, never reaching the base
of the spathe. The seeds are 1 to 2 (rarely 3) per
berry and 0.5—0.7 cm in diameter and are strongly
depressed on both sides with a strongly interrupted
dorsal ridge. The tuber often has many tubercles at
the apex.

About 10 years after the discovery of Dracontium
asperum, a plant corresponding to D. asperum was
redescribed as D. elatum by Masters (1870), based
on a cultivated specimen from William Bull's hor-
ticultural establishment in Chelsea, England. In the
protologue, the origin of the plant was mistakenly
referred to as tropical West Africa, where this strict-
ly Neotropical genus does not occur. This plant was
believed by Masters to have been introduced into
England from Guyana by the British. It is very like-
ly that the plant was distributed by J. J. Linden, a
plant importer and dealer in Brussels, since a fer-
tile specimen (Sanders 1920, K) identified as D.
elatum was prepared later in 1870 from a plant
cultivated at Sanders's nursery and obtained from
"Sauromatum asperum,"

e

Linden under the name
name mistakenly used for D. asperum. This collec-
tion, Sanders 1920 (K), is designated here as the
lectotype of D. elatum because no material exists
from the living collections cultivated by Bull and
because the specimen is believed to be from the
same living plant. Thus, the specimen prepared by
Saunders is preferable to the cited figure 58 in the
protologue.

еп years after the discovery of Dracontium as-
perum, another collection of this species was made
y W. . Im Thurn at Pomeroonon on the Guy-
ana ET of the Corentyne River near the кү
Coast and was subsequently redescribed by J.
Hooker as D. foecundum in 1885.

Additional specimens examined. BRAZIL. Amazon-
as: Yano mami, ч Demini, Watoriketheri, below Serra
ini 1717 (К, MO). DOMINICAN REPUB-
LIC. Duarte: Caño Azul, Villa Rita, Liogier 19363 (NY).
ee Kuyuwini River, 150 mi. from mouth, Smith

3029 (F. GH, 2 U, US). PUERTO RICO. Río Abajo
State Forest, km due S of Camp Radley, Proctor
46104 (SJ); SW 5 Ness: Baja Rd. 155, km 53, elsa
s.n. (NY); San Juan, Barrio Aibonito, Guajatac
e km SW of Rd. 437 & Hd. 113, fae 46460

7. Zh MO); Rfo о оа Station, Brit-
ton ^ Britton 10060 (NY). 1 soca own: Demerara
River, Jenman 6895 (NY
dg District: El Шиш: M z 3420 (US). G UY-

. Sierra de Luquillo: Barrio Mameyes, 0.9 km due
SSE of La Vega, Proc tor 47976 (SJ). SURINAM. Broko-

—

pondo: 2.4 km 5 of Gansee, Feroe Creek, Cup dd 1159
(U). Commewijne: Florschutz & ps as 3162 BÀ Y,
Nickerie: Zuid River, 2 km above mouth of Lu

Irwin et al. 90709 (NY). TRINIDAD & TOBAG О. Trin.
: Buenos Aires, Erin, о 7455 (NY); нуган
Rd., Kalle & Gonzales 1358 (TRIN); Manzanilla to May

aro Rd. at mi. 25, Johnson 243 (TRIN); Nestles Milk Fac-

tory, Barnes s.n. (TRIN 18584); piri Grove, Churchill
Roosevelt Hwy., Boos s.n. (TRIN 31296).

Cultivated plants. Guyana: Ore alls left bank of Cor-
entyne River, cult. Royal Botanical Gardens at Kew, Great
Britain, Im Thurn s.n. (К), Jenman 491 (К); originally
from Leiden Botanical Garden, hort. Saunders, Saunders

) (K). Trinidad: cult. 5 Gardens of St.
уан S. A., Broadway 5212 (F); . a

at Orange Grove Estates in 9 by J. ‚ 1988,
ak at Royal Botanical Gardens at Kew, Gre a ge iM ain, G.
Zhu 1442, 1444, 1479, 1497, 1515 (MO); collected by H.
Boos, Mar. 1993, G. Zhu 1484 (MO); Port of Spain, col-
lected by H. Boos, C. Zhu 1509 (MO). Puerto Rico: cult.
Washington, D.C., Barret s.n. (US)

2

Avis,

—

5. Dracontium bogneri С. Zhu & Croat, sp. nov.
TYPE: Brazil. Rio Sobrado, bei der
Briicke, cultivated at Miinchen Botanical Gar-
den, 1994, J. Bogner 2097 (holotype, MO-
04633684!; isotype, MO-04633683!, RJ!). Fig-
ure 8

Goiás:

Petiolus 1—2 m longus; lamina 50—62 cm longa, 40—50
cm lata; pedunculus subterraneanus, 0-1.5 cm longus;
spatha 2.9-7.3 cm longa, 1.4-2.8 cm lata; extus brunneo-
la; intus velutina, purpurea; spadix 1.2-2 cm longus, 0.5-
0.7 cm diam.; baccae 5 usque 0.8 em diam.;
semina brunneola, usque 0.5-0.6 em diam.

Tuber hemispherical, 8 cm diam., 5 em thick,

flat or slightly sunken above, rounded and whitish
cm below ground level;
id, 0.6-1.2 cm

to pinkish below, 25-3

tubercles few, rounded or obovoid,

diam., borne around the periphery of tuber; roots
0.3 em diam., white, sometimes tinged pink near
the base; cataphylls 1, 24-25 X 2-4 cm, pink,
reaching or surpassing ground level. Leaves soli-
tary; petioles 1-2 m long above ground, 1.2-2 cm

iam. at midpoint, brownish green, contrastingly
mottled with dirty white or pale green blotches and
forming a reptilian pattern, usually with spiny pro-
jections; juvenile blade sagittate, or sagittately
lobed; mature blades spreading horizontally, 0.5-1
m diam., papyraceous, rarely fenestrate, never var-
iegated, without raphide cells or dark markings, se-
miglossy and medium green above, semiglossy and
medium green below; middle division twice trichot-
omously branched, 50-62 cm long, 40-50 cm wide,
with terminal subdivision consisting of 3 sections,
with each basal subdivision consisting of many seg-
lateral divisions twice dichotomously
branched, 0.5-0.6 х 0.4—0.5 cm, with terminal
subdivision consisting of 2 sections, with basal sub-

ments;

division consisting of many segments; terminal and

Volume 91, Number 4 Zhu & Croat 619
2004

Revision of Dracontium

Fi
tuber
Leaf

gure 8.

А
апа inflorescence, — athe cut away to po. the interior of the spathe and the spadix at xd

b lade. —JD.

B

0.5 cm

D. Dracontium bogneri. A—C. Photos by J. Bogner from type, Bogner 2097. —A. Flowering x with

Si
Seeds in sida view (Irwin et al. ЗАТ.

620 Annals of the
Missouri Botanical Garden

0.9 cm

Figure 9. A-D, Dracontium croatii. —A. lı Ylorescence of live type e voucher at anthesis (Croat 72368). —B.
Spathe with one side removed to expose interior and spadix at anthesis. —C. Close-up of infructescence. —D. Seeds
in side view (from Dodson & Fallen 7762).

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

subterminal sections free, each usually consisting
of a single segment: leaf segments often entire or
bilobed, broadly oblanceolate, more than 5 em wide
on each side of the major ribs, ovate-oblong and
lanceolate, mostly free from each other in each di-
vision, often with contrastingly smaller rounded or
triangular segments alternating with larger seg-
ments; apices acuminate, or caudate; ultimate seg-
ments 12—15 cm long, often confluent with penul-
timate segments; other segments 5-8 cm long:
penultimate segments free from subterminal sec-
tions; medial segments confluent with the basal
subdivisions: basal segments present, free from
each other: rachises patterned distinct from petiole.
pale green, tinged brown or similar to petiole but
in much paler shades, smooth: tertiary veins prom-
inent above and weakly raised below: bracteole 1.

1.8-6 x 1.2-2.4 cm,

longer than the peduncle, covering up to % of the
8 | 2 uł

dark brown, the longest one
spathe. Inflorescence solitary, appearing before new
leaf: peduncle 0—1.5 cm long above ground. 0.3—
0.6 cm diam. at midpoint, often almost completely
subterranean, mottled, brownish
smooth: spathe 2.0-7.3 cm long, 1.4-2.8 em wide.
cymbiform. cucullate, arching to 45%, apex acumi-

scarcely green,

nate: inner surface covered with dense, translucent
scales 1-2 mm long, purple-red and olive-brown.
with. translucent area obscure: outer surface olive-
brown, semiglossy or matte; margins entire, broadly
overlapping at the base; veins obscure inside and
raised outside, conspicuously darker or paler than
the spathe, brown: spadix exposed (+). stipitate.
1.2-2 X 0.5-0.7
cm at anthesis, never with appendages at apex:

stipe 0.20.4 X 0.3-0.6 cm at anthesis, light brown
or brown. Flower tepals 4 or 5. 1.5-2 mm long. |
mm wide, light brown; stamens (7)8 or 9: filaments
0.3-3.5 mm long; anthers 0.8-1
pletely exserted: ovary bilocular. pale green: stigma

cylindric, light brown or brown,

mm long. com-

4-lobed: style 1-1.5 mm long above tepals. green-

ое

ish, persistent. /nfructescence with spadix 5.5 X 24
0.8 cm diam.,

cm in fruit; berries 4-seeded. em

thick,

truncate; young berry light green, without reddish

subglobose, 3- to 6-angular, apically sub-
dots and raphide cells; mature berry yellowish or-
ange: seeds 0.5-0.6 X 0.5-0.6 cm, light
brown, laterally depressed: dorsal ridges obvious.

reniform,

3. + continuous, more than | mm thick, finely dec-

orated with small cells on both sides.
с Flowering in November: mature
fruits in January.
e and habitat.
endemic to Brazil in Goiás and adjacent areas in

the states of Mato Grosso do Sul and Рага. It occurs

Dracontium bogneri is

in Premontane moist forest (P-mf) and Tropical mon-
tane wet forest (TM-wf) life zones. at elevations of
300 to 1000 m.

Discussion. Dracontium bogneri has the small-
est spathes in the genus, as small as 2 em long and
1.4 ст wide. It is characterized by having a com-
pletely subterranean peduncle and the inner spathe
surface covered with translucent scales. It is su-
perficially close to D. ulei in having an almost com-
pletely subterranean peduncle, but that species dif-
fers in having laterally convex, smooth seeds (vs.
laterally depressed, finely decorated seeds for D.
bogneri). This species is named in honor of Josef
who in-

Bogner, of the Munich Botanical Garden,

dependently recognized this taxon as an unde-
scribed species at the time that he collected it. He
is one of the foremost aroid specialists in the world,
South

America include the type specimen of this species.

whose significant aroid collections from

Sen s. BRAZIL. Goiás: 14 km S of Niquelándia.
14°2 18°20’ W, 1000 m. H. S. Irwin et al. 34730 (NY).
Minas Гаа Municipo de Itaberiera, road from Itaber—
iera to Claudio, then side road to Serranha, 900 m, 8°58'S,
72 M. in shade of seasonally dry woods, 2 Feb. 1993,
G. Zhu 1510 (MO) [originally collected,

Cultivated plants. Brazil. Para, Cai do Ara-
km W of oe cu Allen Fernandez,
Florida, є * Plour man 12043 (F).

Meerow et al.].

guala, 20
South Miami,
6. Dracontium croatii G. Zhu, Novon 5:
1995. TYPE: Ecuador. Lita-*
km W of Lita, San Lorenzo Cantón, Esmeral-
das, 0°55’N, 78?28'W, 705 m. С. Zhu 1493
(holotype, MO). [Originally collected,
Croat 72368 (MO), cult. at MBC
2p.9

San Lorenzo,

».] Pistes

Tuber hemispherical, 8-11 em diam., 6.5 cm
thick, rounded and whitish to brownish
below. 4-30 cm below ground level; tubercles few,
rounded or cylindrically elongated, 0.5-1
1-2.3 em long, borne around the periphery

flat above,

cm
diam.
of tuber: roots whitish, 2-4 mm diam.; cataphylls З
to 5. 5-45 X 3-5 cm, dark brown or pink, 5-15
em long жн ground, Leaves solitary; petioles 1.4—
3 m long above ground, 2-4.5 cm diam. at mid-
point, dark. green or brownish green, contrastingly
mottled with dirty white or pale green blotches and
forming a reptilian pattern, usually smooth in upper
half and with irregular protuberances in lower half;
juvenile blade sagittate, or sagittately lobed; mature
blades spreading horizontally, 1—1.5 m diam., thinly
coriaceous, rarely fenestrate, never variegated,
without raphide cells or dark markings with abun-
dant raphide cells, semiglossy and dark green
above to matte and medium green above, semiglos-

622

Annals of the
Missouri Botanical Garden

sy and medium green below to matte and medium
green below; middle division twice trichotomously
branched, 0.8-1

division consisting of 3 sections, with each basal

X 0.5-0.8 em, with terminal sub-

subdivision consisting of many segments; lateral di-
visions twice dichotomously branched, 0.8—0.95 х
0.5-0.8 em, with terminal subdivision consisting of
2 sections, with basal subdivision consisting of
many segments; terminal and subterminal sections
confluent, each consisting of many segments;
broadly oblanceolate, more than 5 em wide on each
side of the major ribs, oblanceolate, mostly conflu-
ent with each other in each division or at least some
of the basal segments free from each other, often
with contrastingly smaller rounded or triangular
segments alternating. with larger segments; apices
acuminate, or rarely acute; ultimate segments 20 cm
long, confluent with penultimate segments; other
segments 3.5-15 cm long: penultimate segments
with
segments confluent. with the basal subdivisions:

confluent the subterminal sections; medial
basal segments present, free from each other or
rarely confluent with each other; rachises patterned
similar to petiole but in much paler shades, with
irregular protuberances; tertiary veins prominent
and conspicuous above: bracteoles З or 4, 20 X 2-
4 em, light or dark brown, the longest one much
shorter than the peduncle, confined at the base of
the peduncle. Inflorescence solitary, appearing be-
fore new leaf; peduncle 80-120 cm long above
ground. 1.3-3.5 cm diam. at midpoint, more than
half as long as the petiole, mottled similar to petiole
but deeper in color. brownish green, with irregular
protuberances in lower half and spiny projections:
spathe 23-50 em long. 8-15 em wide, cymbiform,
cucullate, erect or slightly arching, apex obtuse; in-
ner surface velvety, maroon and solid greenish
white (EO cm along the du with translucent
area obvious, 3-7 cm high, 1.5 to 3 times longer
than spadix: outer surface bn yellowish green,
matte; margins entire, broadly overlapping in the
lower two-thirds; veins obscure inside, conspicu-
ously darker or paler than the spathe, purple and
pale green (on lower half); spadix hidden, sessile
1.8-6.5 cm
em diam. at anthesis, never with ap-

„

cylindric, narrower at apex, purple,
long, 0.7-1.5
pendages at apex. Flower tepals (6)7 or 8(9). 1.8—
2.2 X 1-2 mm, brown-purple or dark purple: sta-
mens 6 to 9; filaments 1.5-2 mm long; anthers 1—
1.5 mm long, hidden or slightly exserted; ovary
bilocular, pale green; stigma 2-lobed, or rarely 3-
lobed; style 1-1.2 mm long above tepals, purple.
persistent. /nfructescence with spadix 6-12 cm long,
1-1.8 em

diam., globose, apically rounded: young berry light

3.4—5 cm diam. in fruit; berries 2-seeded,

green; mature berry orange, with or without some
reddish dots or raphide cells; seeds 0.8—1 cm diam.,
rounded, reddish brown, laterally depressed: dorsal
ridges obvious, more than 3, strongly interrupted,
monomorphic, more than 1 mm thick, 1-2 mm
high, smooth on both sides.

Phenology. Flowering from November to Feb-
ruary; mature fruits from February to July.

Distribution and habitat. Dracontium croatii is
known only from the western slopes of the Andes
in Ecuador: it may also occur in adjacent areas in
Colombia. It occurs in Premontane wet forest (P-wf)
and Tropical montane moist forest. (TM-mf) life
zones (Holdridge et al.. 1971), at elevations of 450
to 1000 m.

Local
MO).

Discussion.

names. "Papayucla" (Barfod 41597,
Morphologically, D. croatii does not
appear to be particularly close to any member of
the genus. It is readily distinguished by its showy
greenish spathe that is unique in Dracontium, by
the matte upper leaf-blade surface (typically se-
miglossy elsewhere), and globose mature fruits and
seeds that are up to 1 em in diameter, the largest
in the genus.

This species was named in honor of Thomas B.
Croat of the Missouri Botanical Garden, who served
as the chairman for the first author's dissertation
committee and laid the foundation of this work
through his collections of both herbarium speci-
mens and photographic materials.

еи зеен — ECU, ADOR. Paren
~ Res., Ама Ethnic Reserve, Hoover et a 3279 (QCA);
Marcos-1 Dice. "Barfod 415€ 7 (AAU, d
C. disse: bridge over Río C D near jet.
Rio Baba, 7 km from jct. of entrance rd. at 7 km a
Santo Domingo on ee to Quevedo, ‘Dodson 5951 (SEL);
15 Centinela, at crest of Montafias de Ila on rd. 12 km
from Patricia Pilar i 24 de Mayo, 17 & Fallen 7762
(MO, QCNE, SEL); La Centinela, 13 km E of Santo Do-
Aino Oe vedo Hwy. in Patricia bs Croat 73040 (MO,
QCNE).
rera plants. Ecuador. Cult. by Dewey Fisk, Flor-
ida, U. S. A., C. Zhu 1508 (MO); cult. Marie Se Ьу Воап-
ical ( de ns (75-461. vo
1576 (SEL). \
Botanical Gardens (78-2 EL), Chris-
tenson 1154 (SEL). pie 717 . Plowman 10926
E : Zhu 1453 (MO); cult. MB e hered by Croat
68). G. Zhu 1459, 1518 (MO); received from the Marie
se ih Botanical Gardens (78-2173, vouchered by Dodson
38). С. Zhu 1453, 1495 (MO).

e

tenson

Е
SS
=
522
No
les]
ies]
dg

7. Dracontium dubium Kunth, Ind. Sem. Hort.
Berol. 1844: 283. 1844. Echidnium dubium
(Kunth) Engl., Pflanzenr. 4, fam. 23C: :
1911. TYPE: Pl. 88 in Schott. Gen. Aroid.,

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

623

1858: 88 (neotype. designated by Zhu. Boos
& Croat (1998: 102)): Venezuela. Carabobo:
Caño Paso Ancho, ca. 6 km S of Valencia, near
El Paito, C. S. Bunting 3677B (epitype. des-
ignated by Zhu, Boos & Croat (1998: 102).
MY!: isotypes, MO!, NY). Figure 10.

Dracontium changuango G. S. Bunting, е. 60:
302. 1986. ТҮРЕ: = 'nezuela. Carabo afio Paso
Ancho, ca. 6 km S of Valencia, near El Psi to, 22

. 6. S. Punting & Trujillo 2856 (holotype,

МҮ"; isotypes, MO!, NY!).

I

Tuber hemispherical, 5-17 cm diam., 6-9 em
thick, flat above, rounded and whitish to brown be-
low, 3-36 cm below ground level; tubercles few.
0.5-0.9
diam., 0.5-1.5 cm long, borne around the periphery
of the tuber; roots whitish, 1-2 mm diam.: cata-
phylls 2 or З. 3-36 X 1.5-8 em, pink to light
brown, reaching or surpassing ground level. Leaves
solitary: petioles

rounded or cylindrically elongated, cm

1-2.4 m long above ground. 2—

cm diam. at midpoint, dark green or tinged brown.
contrastingly mottled with dirty white or pale green
blotches and forming a reptilian pattern, smooth or
sometimes with spiny projections; juvenile blade
sagiltate. or sagittately lobed; mature blades spread-
1-1.2

rarely fenestrate,

ing horizontally, diam., subcoriaceous

papyraceous, never variegated,
sometimes with abundant dark markings, semiglos-
sy and dark green above, matte and medium green
below: middle division twice
X 45-75 em, with terminal sub-

division consisting of 3 sections, with each basal

trichotomously
branched, 50-7

subdivision consisting of many segments; lateral di-
50-70 X
7-73 cm, with terminal subdivision consisting of
2 sections,

visions twice dichotomously branched,

N

with basal subdivision consisting of
many segments; terminal and subterminal sections
confluent or free, each usually consisting of a single
segment or a few segments or rarely each consisting
of many segments; leaf segments bilobed, broadly
oblanceolate, more than 5 ст wide on each side of
the major ribs, orbicular-ovate, at least some of the
basal segments free, often with contrastingly small-
er rounded or triangular segments alternating with
larger segments; apices acuminate, or acute; ulti-
mate segments 9-20 cm long. free from penultimate
segments; other segments 10—20 cm long; penulti-
mate segments confluent with the subterminal sec-
tions; medial segments confluent with the basal
subdivisions; basal segments present, free from
each other; rachises patterned distinct from petiole,
pale green or distinct from petiole, pale green.
tinged brown, with irregular protuberances; tertiary
veins obscure above and conspicuous below: brac-

teoles | or 2, 5-15(37) X 1.5-2 cm, white to pink
(at apex), the longest one longer than the peduncle.
covering up to % of the spathe. /nflorescence solitary
or sometimes two, appearing before new leaf: pe-
duncle 3-36 cm long above ground, 0.5-1 cm diam.
at midpoint, often almost completely subterranean
(to a few em above ground level), mottled similar
to petiole but lighter in color. white tinged pink,
smooth: spathe 4-15 cm long. 2-5 cm wide, non-
cymbiform, broadened at a certain point and dif-
erentiated into a proximal tube and a distal lamina
(blade), non-cucullate or cucullate (slightly), arch-
ing to 45°, apex acuminate; 1-4 X 1.8-3.5 cm at
widest point; lamina 2 or 3 times longer than the
tube; inner surface covered with dense, translucent
scales 1-2 mm long, olive-brown or red-purple.
surface ma-
roon, matte; margins entire, broadly overlapping in

with translucent area obscure; outer
the lower third; veins obscure inside and outside,
similar to the spathe in color; spadix exposed (often
extending above the spathe tube), stipitate, cylin-
brownish purple, 1.2—4.2 X 0.5-1.3 cm at
anthesis, often with several appendages at apex.
0.2-0.5 em long when present; stipe 0.2-0.8 X
0.4—0.5 em at anthesis. Flower tepals 6 or 7, 1—2

dric,

mm long, 0.5-1 mm wide, brown-purple; stamens
6 or 7; filaments 0.5-1.5 mm long; anthers 0.8-1
mm long, slightly exserted; ovary bilocular or 3- to
5-locular, pale green; stigma 3-lobed, or 4-lobed:
style 0.2-0.5 mm long above tepals, greenish, not
persistent. /nfructescence with spadix 4-6.5(10) X
2.6—3.5 cm in fruit, berries (1)3- or 4(5)-seeded, 1—
1.2-1.7
apically truncate; young berries dark
green; mature berries orange (or yellow), with or

1.5 em diam., cm thick, subglobose, 3- to

O-angular,

without some reddish dots or raphide cells, seeds
0.8-1 cm long, 0.5-0.7 ст diam., elongated
rounded, red-brown, laterally flattened; dorsal ridg-
es obvious, more than 3, strongly to slightly inter-
rupted, monomorphic, less than 0.5 mm thick, 0.8—
l mm high, smooth on both sides. Chromosome
number 2n = 26 (Aristeguieta 12734; Petersen,
1939

Phenology. Flowering from late January to
April; mature fruits from May to July.

Distribution and habitat. Draconttum dubium
ranges from the Amazon basin to the Atlantic coast
in Venezuela and is expected to be found in adja-
cent areas in Colombia and Guyana. It occurs in
the dee ‘al moist forest (T-mf) life zone (Holdridge

et al., 1971), at elevations of 80 to :
"m names. “Changuango” (Bunting 4432,
MY); “cuma pan" (Liesner & González 5773, MO).

Discussion. Draconttum dubium is character-

Annals
мое ДР Garden

Figure 10. A-D, Dracontium dubium. —A. Leaf of ld plant at Munich Botanical Garden (Aristeguieta
12734). —B. Seeds in various юла (Huber 1826). —C. Inflorescence at anthesis (Aristeguieta 1273
Е

specimen of D. changuango С.

zunting (Bunting & Trujillo 2 2850).

). —D. '

ype

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

ized by having the inner surface of the spathe cov-
ered with dense, translucent scales (1-2 mm long)
and a spadix that often has apical appendages. Dra-
contium purdieanum is very similar in terms of its
leaf. the relatively short inflorescences, the non-
cucullate spathe. and the occasional presence of
appendages on the end of the spadix: it differs in
having usually shorter peduncles (less than 5 cm
above the soil) and in having seeds with three con-
tinuous ridges to 0.5 mm high.

Dracontium dubium Kunth was first collected by
Richard Schomburgk during an expedition to Brit-
ish Guiana (Guyana) in 1840-1844 at the base of
Mt. Curassawaka of the Kanuku Mountains, south
of Nappi. and several living tubers were sent to the
Botanical Garden of Berlin in 1843 (Roth, 1922:
307—380: 1923: 103). One plant bloomed in the
Garden and was described by Kunth in the follow-
ing year (Kunth, 1844). Schott (1860: 481) noted
that there were fertile collections of this species а!
the Berlin Herbarium (B). However, no specimen
39).
Garten zu Berlin

of D. dubium was seen by Engler (in 1911:
who only cited “Bluehte im Bot.
Sept. 18447 (flowered in Berlin Botanical Garden
in September 1844) Schott
(1860) might very likely have only seen live spec-
imens of the species since at Kunth’s time, garden

under the species.

plants were often described and illustrated without
preparing herbarium specimens (Paul Hiepko, pers.
comm.). Kunth had apparently made a drawing of
the inflorescences and some floral details of the
species, which was deposited in the Berlin herbar-
1911: 38, fig. 14A—F). More than a
decade after the discovery of D. dubium, Schott
(1857b). based on unspecified ovary and stigma de-

ium (Engler.

tails of the species, described the new genus Echid-
nium. giving the single species a new name, E.
schomburgkii. In the following year, Schott (1858b:
pl. 88) published a plate that included the inflo-
rescence and floral details of this species under the
name H. schomburgkii. which copied Kunth's draw-
ing adding an inflorescence at anthesis and other
floral details. Later. when he published the first
comprehensive classification of the Araceae, Schott
(1860)
D. dubium as a synonym. Under contemporary rules
of the ICBN (Greuter et al., 2000), . schomburgkii
is a superfluous name, since Schott should have
used the name E. dubium for the transfer. Engler
(1911) rectified this situation. by publishing the
combination E. dubium (Kunth) Engl.

Echidnium is ostensibly distinguished from Dra-
having a unilocular ovary with two

accepted the name E. schomburgkii, citing

contium by
ovules (Schott, 1857b), as opposed to a bi- or plu-

rilocular ovary in Dracontium. However, these

characters have been shown to be either spurious
(Zhu, 1995) or not to be good generic characters in
this group (Bogner, 1985; Hay, 1988; Zhu, 1996).
The two plates originated from the typical material
of D. dubium (Genera aroidearum, pl. 88, Schott,
1858b: Das Pflanzenreich, 4 (23€): p. 38, fig. 14A—
F, Engler, 1911) clearly demonstrated a plant of at
least two locules. Schott’s statement of a unilocular
ovary was evidently erroneous based on his own
illustration. Zhu (1995, 1996) noted that unilocular
ovaries do not occur in Dracontium and this genus
never has more than one ovule in each locule; these
stand as generic traits of the genus. Therefore,
Echidnium was accepted as a synonym of Dracon-
пит. and D. dubium is the accepted name for the
treated species (Zhu et al., 1998)
Idditional E ps I VENEZUELA. Ama-
zonas: alreded 1 Juan de Manapiare, Girardi 16
(VEN): parte я phe iA lower Río Ventuari, 20 km E of
confluence w Río Orinoco, Huber 1826 (MO); Santa Bárbara
del Orinoco, near confluence of Río Orinoco and Río Ven-
117171 (MO, VEN); Atures, Isla
Castillito-San Fernando de Atabapo on Río Orinoc 0. out-
skirts of Siquita, Bunting 3677A (MY, NY); Caño Месіі.
upper Py Ventuari, Lister 461 (K). Apure: Río Orinoco to
Piedra La Villa, poss Raudal Marimare, big. Ф
жер ino 11392 (М Barinas: Res. For. Ca
Cantón, Meier 435 (VEN).
Lr Liesner м Gonzdlez 5773 (MO, VEN)

. tributary v Канай, Steyermark et
al. 131647 (MO). Carlota: Caño Paso Ancho, 5-6 km
S of peo ‘ia on rd. to El Paito, Bunting & Trujillo 28: E
её МҮ, Cojedes: Quebrada Chumeo, Fundo La
ona, De Dar 6818 (VEN). Guárico: Río Orituco. S of
(ам. e 260 (VEN): Calabozo, Aristeguieta 5381
Fundo у

luari, Steyermark et al.

tuguesa: Guanare,

<

k
mu 1 (МО, PORT,
Rio Tucupido, Rodriguez 158 (MY ); Turen, Esta. de S lvi

Aristeguieta ee (МО, PORT); Pozo
‚ Ortega 748 (MO, PORT)

P ulti nied bu Venezuela. Portuguesa, Turén (Villa
Bruzual), cult. Munich Botanical Garden, Germany, Aris-
teguieta 12734 (M); Amazonas, Atures, Aragua, Mara
along the Río Orinoco, collected by G. S. Bunting, Bun.
ting 3077A, Bunting 367 7B (NY).

8. de gigas (Seem.) Engl.. Monogr.
Phan. 2 . 1879. Godwinia gigas Seem.. :
Bot 313. t. 96, 97. 1869. TYPE: Fig. li

t. 96 & 97, 1869 (lectotype, he
nated by Zhu (1994a: 407)); Nicaragua. Chon-
tales: betw. Javalf Gold Mine & Quebrada de
Las Lajas, 19 Mar. 1884, Brown s.n. (epitype.
designated by Zhu (1994b: 407), K!). [Cull. at
К, originally collected by B. Seemann.] Fig-

ures 2C, 11, 14D
12 cm

Tuber hemispherical, up to 20 em diam.,

626 Annals of the
Missouri Botanical Garden

|
Figure 11. A-D, Dracontium gigas. —A. Plant а natural habitat at La Selva in Costa Rica (photo by С. С.
В ай, —B. Flowering plant at anthesis with М. Н. Grayum at La Selva (Grayum 7911). —C. Inflorescence at

Flow
anthesis showing interior of spathe with spadix at d sis. —D. Seed showing side view (Beach 1490).

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

627

thick, flat above, rounded and white to brown be-
low, 5-60 em below ground level; tubercles few.
0.5-1 1-2 cm,
around the periphery of tuber; roots 0.4 cm diam..

cylindrically elongated, borne
white: cataphylls 4 to 7, up to 40 em long (to 5 em
long above ground level), 4—10 cm wide, pink to
light brown (when dry). Leaves solitary or sometimes
two or more per tuber; petioles up to 3.4 m long
above ground, up to 9.5 em diam. at midpoint, dark
green, contrastingly mottled with dirty white or pale
green blotches. usually smooth in upper half and
with irregular protuberances in lower half; juvenile
blade sagittate, or sagittately lobed; mature blades
spreading horizontally, 1.5-2.5 m diam.. subcoria-
ceous, rarely fenestrate, never variegated, without
raphide cells or dark markings, glossy and medium
green above, semiglossy and medium green below:
more trichotomously

middle PES j times or

branched, ! 1.8 em, with terminal subdivision
consisting E 3 sections, with each basal subdivi-
sion consisting of many segments: lateral divisions
1.3 * 1.6

em, with terminal subdivision consisting of 2

3 times or more dichotomously branched,

зес-

tions, with basal subdivision consisting of many
segments: terminal and subterminal sections con-

fluent, each consisting of many segments: leaf seg-
ments often bilobed or rarely trilobed. oblanceolate
or triangular, mostly confluent with each other in

each division, often with contrastingly smaller

rounded or triangular segments alternating with
larger segments; apices often caudate, or sometimes
acute; ultimate segments 10-16(220) em long. con-
fluent with penultimate segments: other segments

10-20 em

with the subterminal sections;

long: penultimate segments confluent

medial segments
confluent with the basal subdivisions: basal seg-
ments present, confluent with each other; rachises
patterned similar to petiole but in much paler
shades, smooth; tertiary veins conspicuous above

З ог 4. 10-60 х
5-10 ст above ground level) 4-6 cm.

and obscure below: bracteoles
(sometimes
light brown. the longest one much shorter than the
peduncle, confined at the base of the peduncle. /n-
florescence solitary, appearing before new leaf: pe-
duncle 30-120 cm long above ground. 3.5-6 cm
diam. at midpoint, less than half as long as the
petiole, mottled similar to petiole but deeper in col-
or. dark green or brownish green. with irregular
protuberances in lower half: spathe 58-78 х

15(-21) em, eymbiform, cucullate, erect or slightly
arching, apex obtuse: inner surface semiglossy, red-
purple or purple-red, with a translucent area ob-
vious, 4—6.5 em high, shorter than spadix; outer
surface maroon tinged brown, matte; margins en-
tire, broadly overlapping in the lower two-thirds:

veins purple, obscure inside and outside (slightly
impressed inside), conspicuously darker or paler
than the spathe on top; spadix hidden, sessile or
stipitate, cylindric, brown-purple, 9-16 X 1.5-1.8
cm at anthesis, never
Flower tepals 6 to 8(9), 1.5-2 mm
wide, light brown tinged green: stamens 8 to 17(19):

with appendages at apex.
3.5—5 mm long.

filaments 1-3.5 mm long; anthers 1—1.5 mm long.
completely exserted: ovary 3- to 4-locular, pale
green; stigma 3-lobed: style 4-6 mm long above
tepals, dark purple, persistent. /nfructescence with
spadix 20-30 cm ep 4-6 cm diam. in fruit; ber-
8 X 1.5 cm.
or globose (rarely), sin truncate; young berry
unknown;

ries often 2-seeded, 1- to 5-angular

mature berry orange or purple-brown,
with or without some reddish dots or raphide cells;
seeds 1—1.2 cm diam., rounded, reddish brown, lat-
erally raised: dorsal ridges obvious, 3. continuous,
less than 0.5 mm thick. Chromosome number 2n =
20 (Bogner 1267; Petersen, 1989)
Phenology. Flowering from December to April:
mature fruits from April to August.

Distribution and habitat. Dracontium gigas
ranges from central Nicaragua (Chontales). along
the Atlantic slope to central Costa Rica (Heredia.
Limón). It occurs in Tropical moist forest (T-mf) and
Premontane wet forest (P-wf) life zones (Holdridge
et al., 1971). at elevations of 15 to 100(—150) m.
Discussion. Dracontium gigas has the largest
to 78 cm
long and 13 to 15(-21) em wide. It is the most well-

spathes in the genus, ranging from 58
D O

known species horticulturally, especially in Europe.
It regularly blooms in European gardens and pri-
vate nurseries, but has never been reported flow-

ering in gardens of the New World. This species
propagates rapidly by means of tubercles. It is also
a fast grower, capable of growing a couple of inches
in height overnight. It is often a big attraction when
it blooms.

Dracontium gigas is easily confused with D. pit-
tieri in sterile condition. The mature leaves of these
species are almost identical. However, leaves of D.
pittieri tend to have more raphide cells, especially
when voung. and less leaf tissue along the rachis
and at the branching points. The upper half of the

4

petiole is often smooth and unicolored in D. pittieri,

—

while often mottled and with projections in D. gi-
gas. Despite strong vegetative similarities, these
two species are distinct in their inflorescence mor-
phology. Dracontium gigas has a large spathe and
a short peduncle, which is always less than twice
as long as the spathe. Dracontium pittieri has a
much longer peduncle, 5 to 8 times longer than the
spathe. The spathe of D. gigas is more or less hood-

628

Annals of the
е Botanical Garden

ed at the apex, with the margins broadly overlap-
ping and completely covering the spadix. The
spathe of D. pittieri is open at the apex with the
margins scarcely overlapping, such that the spadix
is exposed. The translucent area at the base of the
inner spathe surface extends much higher than the
spadix in D. pittieri, while it never exceeds the
height of the spadix in D. gigas (Zhu, 19944).

Since there is no type designated in the proto-
logue of Godwinia gigas Seem., the basionym of
Dracontium gigas (Seem.) Engl.. a plate from the
original material, fig. 1 in J. Bot. 7: t. 96 & 97,
1869, was designated as the lectotype of Godwinia
gigas (Zhu, 1994a). Since this lectotype does not
contain enough information to identify D. gigas
from D. pittieri, a fertile specimen prepared by N.
E. Brown (Brown s.n., К) was designated as an ep-
itype for D. gigas to ensure the accurate application
of these names (Zhu, 19944).

Additional specimens examined. COSTA RICA. Val-
erio 678 (MO). Alajuela: Canas-Upala, Rio Zapote, 1.8-
5 km 5 of Río Canale P CH & Baker 9999 (F, MO,
US); San Carlos, Roig ‚ F). Heredia: Braulio Car-
rillo, Rara Avis, tra iT Bi x tajo and Catarata, G. Zhu 1154
(MO); La Selva, Beach 1490 (DUKE, MO); Río Sarapiquí
at Chilamate, Croat 68381 (B, M, MO); : Sarapiquí, near
Puerto Viejo, Valerio 24 (USJ), 15 Aug. 1993, >. Zhu
I. s (MO). Limón: 10 km NW of Guápile s. Gómez 18513

QO); Río Reventazón below Cairo, Standley & Valerio
da., La Suerte, 29 air
MO, RSA): ш

=

—
—
—
=
=
=
—
an
=
—
e
z

—

=

AGUA. Chontales: sp Re fr LM teh in spinis
(on sheet #6 of Brown s.n., 30 Dec. 1878), p s.n.
Río San Juan: Caño C пре ño, 20 km NE of El €
tillo, Neill & Vincelli 3512 (MO); Res. Indio-Maiz, San
Juan del Norte, Río Indio, Rueda et al. 8615 (MO): El
veg ape comarca Las Maravillas, Rueda et al.
9 (MO), 5225 (MO). Zelaya: Cerro rre i José

л. Са año Sucio-Loma Molle):
; Stawas, | km N of Río Cade de M
km N of La Cruz, Neill 43:336 (MO); drainage of Ríos Punta
Gorda, Alemán and Zapote, Shank & Molina 4953 (GH,
US); E of comarca del $ — el León, Rueda et al. 3390
MO); Mun. Nueva Guin: “Res. Indio-Maiz, Rueda et al.
10190 (МО); este del collado de Nueva Atlanta. Rueda
el al. 3295 M MO).

d d plants. Nicaragua. Cult. at n rlin Botanical
Garden, Germany, Anonymous s.n. (М); Chontales,
nally collected by Seem; ann, W. Bull’s E be-
tween the Javalf Gold Mine and the Quebrada de Los
ajas, cult. Royal Botanic ‘al Gardens at Kew, Great Brit-
ain, Brown s.n. (GH, K), Brown s.n. (GH), Brown s.n. (K).
Costa Rica. Limón, originally collected by M. Birdsey,
cult. at jsi rt and = rine Wilson Botanical Garden at

—

origi-

Las Cruces, G. Zhu 6 (МО); originally collected by
Clarence Abs 'h, is de between San Carlos & San Pe-
dro Cutris, cult. at Munich Botanical Garden, Bogner

1267 (M);
San Carlos, betw. Vasconia and S

MBG, Croat 71840 (MO),

EE collected by Banta, | ¡peta de
ı Pedro Cutris, cult.

Zhu 1156.

1 by С.

MO): vouchered by C. Zhu 1159, 1467 ы
vouc diu by Croat 68381, G. Zhu 1481 (B. М, MO

—

- Dracontium grandispathum G. Zhu & Croat,
РЕ: Ecuador. Napo: Cañon de los
Monos, 15 km N of Coca near Río Coca, Ha-
cienda of Hector Noboa, 0°20'S, 77%01W, 250
n, 9 Apr. 1985, W. Palacios, D. Neill, M. Bak-
er & J. Zaruma 311 (holotype, MO!). Figure
12

sp. nov.

Petiolus 1.25-2.75 m longus; lamina 5 55-15 em longa,
55-00 em lata; pedunculus 1—1.35 m longus, 1.5-2 em
deus spatha 45-50 em longa, 10-15 em lata, cucullata
extus impolita, olivacea; intus velutina, purpurea:
—] em diam.; tepala 5-6; sem-

yasi;
spadix 3-5.5 cm longus, (
ina rubra, 0.6-0.7 diam.

Tuber hemispherical, 10-18 em diam., 6-10 cm
thick, flat above, rounded and white to brown be-
low, 12-20 cm below ground level; cataphylls 3 to
4, 12-21 X 2-3 cm, light brown, reaching or sur-
passing ground level. Leaves solitary; petioles 1.25-
2.75 m long above ground, 2-3.5 ст diam. at mid-
point, dark green, contrastingly mottled with dirty
white or pale green blotches and forming a reptilian
pattern, usually smooth in upper half and with ir-
regular protuberances in lower half; juvenile blade
sagittate, or sagittately lobed; mature blade spread-
1-1.2 m

never variegated,

ing horizontally, diam., subcoriaceous,

sometimes fenestrate, without
raphide cells or dark markings, glossy and medium
green above, semiglossy and medium green below;
middle division twice trichotomously branched, 55—
75 X 50-60 cm,

sisting of three sections, with each basal subdivi-

with terminal subdivision con-

sion consisting of many segments; lateral divisions
55-15 X
em, with terminal subdivision consisting of 2 sec-

twice dichotomously branched, 55—00
tions, with basal subdivision consisting of many
segments; terminal and subterminal sections often
confluent, each consisting of many segments; leaf
segments often entire, broadly oblanceolate, more
than 5 em wide on each side of the major ribs,
ovate or lanceolate, mostly free from each other in
each division, often without contrastingly smaller
rounded or triangular segments; apices acuminate;
ultimate segments 25-30 cm long, often free from
penultimate segments; other segments 15-20 cm
long; penultimate segments free from subterminal
sections; medial segments confluent with the basal
subdivisions; basal segments present, free from
each other; rachises patterned similar to petiole but
in much paler shades, smooth; tertiary veins con-
spicuous above and weakly raised below; bracteoles
3 or 4, 12-22 X 2-3 cm, light brown, the longest
one much shorter than the peduncle, confined to

Volume 91, Number 4 Zhu & Croat 629
2004 Revision of Dracontium
Figure 12. A-D, Dracontium grandispathum. A, B. (C 5 75207). — &. Inflorescence, side view. —B. Close-up E

inflorescence showing

front. viev

у of spathe

with gel IX. —

Pu ikley ). (Cerón & Cerón 3070). Seeds in side

1. (Pinkley 60-B). Immature

infructescence

. Photo by |

630

Annals of the
Missouri Botanical Garden

the base. Inflorescence solitary, appearing before or
after new leaf; peduncle 100—135 cm long above
ground, 1.5-2 em diam. at midpoint, more than half
as long as the petiole, mottled similar to petiole but
deeper in color, brownish green, smooth or spiny
10—15 em,
biform, constricted at a certain point and differen-

projections; spathe 45-50 X non-cym-
tiated into a proximal tube and a distal lamina
(blade), cucullate or non-cucullate, erect or slightly
arching, apex acuminate (very broadly); 10-15 х

0—15 cm at widest point; lamina 2 to 3 times long-
er than the tube; inner surface semiglossy, maroon
or purple-red or olive-brown, with translucent area
em high, 1.5 to 3

times longer than spadix; outer surface olive-brown

moderately conspicuous, 12—15

or green or green tinged brown, matte; margins en-
tire, broadly overlapping at the base; veins con-
spicuous inside and raised outside, conspicuously
darker or paler than the spathe, purple; spadix hid-
den, stipitate, cylindric, pale green or light brown,
3-5.5 X 1-5
ages at apex; stipe 0.5-1 X 0.5-0.7 cm at anthesis,

cm at anthesis, never with append-

light brown or dark purple. Flower tepals 5 to 6,
1-3 mm long, 1-2 mm wide, light brown or purple;
stamens 7 to 11; filaments 1—2 mm long; anthers
0.5 mm long, hidden or slightly exserted; ovary 3-
locular, pale green; stigma unlobed, or 3-lobed;
style 0.5-1 mm long above tepals, dark purple, per-
sistent. Infructescence with spadix 12-18 X 2.5-3.5
em in fruit; l- or 2-seeded, 0.5-0.6 cm
diam., 0.8-1 cm thick, obliquely obovoid, apically
rounded; young berry light green; mature berry or-

berries

ange, without reddish dots and raphide cells; seeds
0.6-0.7 em diam., rounded, red-brown, laterally
flattened; dorsal ridges obvious, 3, often strongly
interrupted, with the central ridge contrastingly
raised, more than 1 mm thick, 0.1-0.2 mm high,
warty along ridges.
Phenology. Flowering from November to May;
mature fruits from March to December.
Distribution and habitat. | Dracontium grandis-
pathum is known only from Amazonian Ecuador
(Morona-Santiago, Napo, and Pastaza). It occurs in
Premontane moist forest (P-mf) and Tropical mon-
tane moist forest (TM-mf) life zones (Holdridge et
al., 1971) at 250 to 1200 m.
Local names. “Nantaymo”
"pitalala para" (Jipa et al. 968,
Discussion.

(Aulestia 1823, MO);

Dracontium PRE oni is veg-
etatively similar to the sympatric D. spruceanum,
r (hence, the
name grandispathum) and usually Hoodia spathe
45-50 X 10-15 ст versus 20-35 X 3-6 cm in
spruceanum. The spathe of D. grandispathum is of-

but differs in having a much a large

E

ten abruptly acuminate apically and that of D. spru-
ceanum is gradually acuminate apically.

Paratypes. ECUADOR. Pp Méndez-

Morona, km 45-6: 756 (MO). Napo:
г N of Jondachi, Harling & Andersson
16404 (GB); ови -Соса, 18 km Е of Narupa, Hammel
& Wilder 17283 (MO); Cantón Lago Agrio, Р ар Dur-
efio, Cofán-Dureno, Cerón & Cerón 3070 (MO, QCA); Dur-
eño, Pinkley 60 (ECON); Cantón Tena, Jatún Sacha, Pa-
lacios 4242 (MO); Par. Nac. Yasunf, Carretera Maxus, km
1, Pompeya, Aulestia 1823 (MO, QCNE); Yasuní, Añangu,
Luteyn et al. 9021 (MO, OCA) Río Tiputini, NW of con-
fluence of Río Tivacuno, Romoleroux 2110 (QCA), 2135
(QCA), 2360 a A), 2649 (QCA); San José de Payamino,
km W of Coca, 1 75 et al, 968 (F). Pastaza: Montalvo,
Rio Bobonaza, 1 & Molau 13549 (AAU). Pichin-
cha: Cantón-Santo Domingo de los Colorados, Cerón et al.
29051. 0 JAP).

Cultivated plants. Ecuador. Napo, Tena, 27 May 1993,
collected by Scott Hyndman, vouchered as J. B. Croat
75207 ; G. Zhu 7528 (MO); vouchered by Pinkley
60, 5 55 204 (ECON), cult. at MBG

10. Dracontium grayumianum G. Zhu & Croat,
sp. nov. TYPE: Panama. Darién: near Par.
Nac. Darién, 4 km NE of Piji Vasal village,
dede W of ANCON a Station,
8°04'N, 77%46'W, 100 m, 27 July 1994, G.
Zhu € T. B. Croat 1506 po EE MO!; iso-
types, B!, Fl, G , M!, NY!, PMA!, SCZ!,
SEL!, UC!, US!). in ID, 2A, 13.

Petiolus 1-2.2 m longus; lamina 0.8-1 cm longa, 0.7—
1 ст lata; pedunculus 1-10(-30) ст 5 0 55 1-1.8 em
diam.; spatha (6)9—15 cm longa, 2.5—4 cm lata, cucullata
asi; extus impolita, pu intus йе жн ригригеа;
spadix 2-3.5 cm lon cm diam.; baccae 1-2
cm diam.; semina bonds 0. 8-1 cm longus, 0.6-0.7
cm diam

Tuber hemispherical, 10-18 cm diam., 6-10 cm
thick, flat above, rounded and white to brown be-
low, 10-20 cm below ground level; tubercles few,
1-3 cm
long, borne around the periphery of tuber; roots
white to 0.4 cm diam.; cataphylls 3, 10-30 X 5-8
cm, white or pink and light brown, 5-15 cm long

cylindrically elongated, 0.8-1.2 cm diam.,

above ground. Leaves solitary; petioles 1—2.2 m long
above ground, 2-6 cm diam. at midpoint, dark
green, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern, usu-

er half; juvenile blade sagittate,
or sagittately lobed: mature blade spreading hori-
zontally, 1-1.5 m diam., papyraceous, sometimes
fenestrate, never variegated, sometimes with abun-
dant raphide cells and dark markings, glossy and
dark green above, semiglossy and medium green
below; middle division 3 times or more trichoto-
mously branched, 0.8-1 х 0.7-1 ст, with terminal

Volume 91, Number 4 Zhu & Croat
2004 Revision of Dracontium

Figure 13.

n side view

A-D, Dracontium grayumianum, type specimen (С. Zhu & Croat 1506

).

0.6 cm

—A. Inflorescence at anthesis
ly

—B. Tube r, petiole ин ‚ апа cluster of immature infructescences. —C. Spadix with mature berries, most
Be 'ady falle n. —D. Seeds in side view

Annals of the
Missouri Botanical Garden

subdivision consisting of 3 sections, with each bas-
al subdivision consisting of many segments; lateral
divisions 3 times or more dichotomously branched,
0.85-1 X 0.7-1.1 em,
consisting of 2 sections, with basal subdivision con-

with terminal subdivision

sisting of many segments; terminal and subterminal
sections free, each consisting of many segments;
leaf segments bilobed, broadly oblanceolate, more
than 5 cm wide on each side of the major ribs,
lanceolate, mostly free in each division, often with
contrastingly smaller rounded or triangular seg-
ments alternating with larger segments; apices acu-
minate, or acute, or caudate (rarely); ultimate seg-
ments 12—15
segments (often); other segments 6-16 cm long:

em long, confluent with penultimate

penultimate segments free from subterminal sec-
tions; medial segments free from basal subdivi-
sions; basal segments present, free from each other;
rachises patterned similar to petiole but in much
paler shades, with spiny projections: tertiary veins
conspicuous above, or weakly raised below; brac-
teoles 5-15(-35) ст long, 2-3(-5) em wide, light
brown, the longest one longer than the peduncle.

covering the basal half or more of the spathe (often).

po

Inflorescences solitary or sometimes two, appearing
before new leaf; peduncle 1-10(-30) ст long above
ground, 1—1.8 em diam. at midpoint, often almost
completely subterranean, scarcely mottled, whitish
tinged pink or gray or whitish green, smooth: spathe
(6—)9—15 X 2.54 em, non-cymbiform, constricted
at a certain point and differentiated into a proximal
tube and a distal lamina (blade), cucullate, arching
457-90", apex acuminate; 2.5-3
est point; lamina similar to the tube in length, or 3

х 2-3 cm at wid-

to 5 times longer than the tube; inner surface se-
miglossy, maroon, with translucent area obscure:
outer surface maroon or olive-brown, matte; mar-
gins entire, broadly overlapping at the base; veins
obscure inside and raised outside (slightly). con-
spicuously darker or paler than the spathe, purple:
spadix Pp uei stipitate, cylindric, brown or pur-

ple, 223.5 x 0.8-1.3

with one to a few appendages at apex, 0.3—0.5 cm

cm at anthesis, sometimes
long when present; stipe 0.5-2 cm long, 0.5-1.5
em diam. at anthesis, brown. Flower tepals 5 to 7.
1—4 mm long, 0.5-1 mm wide, light brown; stamens
(5)6 to 8; filaments З mm long: anthers | mm long.
slightly exserted; ovary bilocular, pale green: stig-
ma 2-lobed; style 1-2 mm long above tepals, dark
purple, persistent. Infructescence with spadix 8—15
cm long, 3.5-5.5 em diam. in fruit; berries 4-seed-
1-1.2 em thick,

vate, apically truncate; young berry light green; ma-

ed, 1-2 em diam., narrowly cla-

ture berry orange, with or without some reddish

dots or raphide cells; seeds 0.8-1 ст long, 0.6-0.7

cm wide, reniform, light brown, laterally flattened:
dorsal ridges obvious, 5 to 6, strongly interrupted,
monomorphic, less than 0.5 mm thick, 1.5-2 mm

high. smooth on both sides.

Flowering from March to April

(June); mature fruits from March to August.
Distribution

Phenolog y.
and habitat. Dracontium grayu-
mianum ranges from southern Panama (Darién and
San Blas) to the central Pacific coastal region it

=

Colombia (Chocó and Valle). It occurs in the Trop-
ical wet forest (V-wf) life zone (Holdridge et al.,
1971) at elevations of 5 to 100 m.

Discussion. Dracontium grayumianum is clos-
est in appearance to D. soconuscum, especially in
leaf size, shape, and form as well as a similar in-
florescence; however, D. soconuscum differs in hav-
ing seeds with 3 very short (0.1—0.5 mm high), dor-
sal ridges instead of 5 to 6 strongly interrupted
(1.5-2 mm high) dorsal ridges.

The species honors Michael H. Grayum of the
Missouri Botanical Garden, an aroid specialist, and
one whose familiarity with the many aspects of
plant taxonomy helped immeasurably with the com-
pletion of this work on Dracontium.

Paratypes. COLOMBIA. Chocó: Río Bicordó,
above Noanamá, Forero et al. 4718 (COL); Río Ca-
carica, Romero 6357 (COL); Río San Juan, near
Palestina, Forero et al. 3800 (COL); Zona de Urabá,
Cerros do Cuchillo, Camino Cuchillo Negro a Cum-
Cárdenas 1805 (JAUM). Valle:
Chocó region, Río Calima, La Trojita, Cuatrecasas
16474 (F); Finca La Cabaña, camino a la Patricia,
Rentería 4314 (JAUM); Finca La Cabaña. Camino
al Río León, Rentería 4220 (JAUM). PANAMA.
Darién: Piji Vasal, C. Zhu & Croat 1507 (MO);
Pinogana, E of El Real, Pittier 6546 (US); Río Chu-
cunaque, Yaviza, Quebrada Barbua, Stern 93 (GH,
MO); km 16 to Yaviza along Q Uvital off Río Chu-
cunaque, Duke 5103 (GH, MO). San Blas: Río
Cangandf, Pueblo Cangandí, Herrera 252A (MO).

bre Noroeste rd.,

—

11. Dracontium guianense С. Zhu & Croat, sp.
TYPE:
Quest de Trois Sauts Crique Euleupousing,
Saut Beco, 15 July 1975, J. de Granville &
Cremers 1129 (holotype, CAY!). Figure 14А,
B, С.

nov. French Guiana. Haut Oyapock,

Petiolus usque 2.5 m deg lamina 40—50 cm longs
35-40 cm lata; p ulus 3040 «

dans spatha 9-10 c

purpurea; intus ve Ши; ршен spadix 2
0.6 em diam.; baccae 0.7—1 ст diam.; semina fusca, 0.65

cm diam

em below ground

Tuber hemispherical, 10—15

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

633

Figure 14. "i C. Dracontium guianense.

—A.

Holot
1129, CAY). —B. Close-up of inflorescence from de Granville & Cremers 1129 (CAY). —C. Infri

type specimen, leaf and inflorescence

fruits (Grenand dies —D. D. gigas. Leaf of plant at La Selva. Heredia Prov.. Costa Ric:

(de Granville & Cremers
ructescence with mature

Annals of the
Missouri Botanical Garden

level: petioles 2.5 1.2 cm

diam. at midpoint, dark green, contrastingly mot-

long above ground,

tled with dirty white or pale green blotches and
forming a reptilian pattern, smooth: mature blades
80-100 em wide,

never variegated,

subcoriaceous, rarely fenestrate,

without raphide cells dar

markings. glossy and dark green above, semiglossy
middle division once or
10-50 x 3540

with terminal subdivision never divided into

and medium green below:
twice trichotomously branched,
em,
sections, with each basal subdivision consisting of
segments: lateral divisions twice dichoto-
10-45 X 3540 cm,

sections,

many
mously branched. with ter-
minal subdivision consisting of 2 with
basal subdivision consisting of many segments; ter-
minal and subterminal sections free, each consist-
ing of many segments; broadly oblanceolate, more
than 5 em wide on each side of the major ribs,
oblanceolate, mostly free from each other in each
division, often with contrastingly smaller rounded
or triangular segments alternating with larger seg-
ments; apices acuminate; ultimate segments 15-17
em long, free from penultimate segments; other seg-
ments 3-15 cm long; penultimate segments free
from subterminal sections; medial segments free
from basal subdivisions; basal segments present,
free from each other; rachises patterned similar to
petiole but in much paler shades, smooth; tertiary
veins obscure above and weakly raised below; brac-
1, 10-15 em long, 0.5-1 em wide, light
brown, the longest one much shorter than the pe-
duncle, confined at the base of the peduncle. /nflo-
rescence solitary, appearing after new leaf; peduncle
30—40 cm long above ground, 0.5 cm diam. at mid-
point, less than half as long as the petiole, mottled

teoles

similar to petiole but deeper in color, brownish
green, smooth; spathe 9-10 X 4-5 cm, cymbiform,
non-cucullate, erect or slightly arching up to 45°
angle, apex acuminate; inner surface semiglossy,
maroon, with translucent area obscure; outer sur-
face maroon tinged brown, matte; margins entire,
hardly overlapping at the base; veins obscure or
conspicuous inside, conspicuously darker or paler
than the spathe; spadix sessile, cylindric, brown or
brown-purple, 2.8 X 0.6 em at anthesis, never with
appendages at apex. Flower tepals 4 to 5, 2-3 mm
long, 1-2 mm wide, light brown; stamens 4 to 6;
filaments 2-3 mm long; anthers 0.5 mm long, com-
pletely exserted; ovary bilocular, pale green; stigma
2- or 3-lobed; style 0.5 mm long above tepals,
green, persistent. Infructescence with spadix 4.3 cm
long, 3.2 cm diam. in fruit; berries 2-seeded, 0.7—

| em diam., 1 em thick, subglobose, 3- to 6-an-
gular, apically truncate; young berries medium

green; mature berries orange, without reddish dots

and raphide cells: seeds ca. 0.65 ст diam., round-
ed, dark brown, laterally convex: dorsal ridges ob-
vious, mm thick. 0.1

mm high. finely decorated with small cells (pits) on

3. continuous, more than

both sides.

Phenology. Flowering known only in July: ma-
ture fruits are known only in May.
Distribution and habitat. Draconttum gui-

anense is known only from the type locality in
French Guiana near the border with Brazil (Para):
it will likely be found in Brazil.
Tropical moist forest (T-mf) life zone (Holdridge et
al.. 1971) at ca. 100 m.

Local names. “M у kala”
mers 1129, CAY)

Dracontium guianense is very sim-

It occurs in the

(de Granville & Cre-

Discussion.
ilar to D. polyphyllum, but differs in having a much
longer peduncle (more than 30 cm above ground
level).

Paratypes. FRENCH GUIANA. Haut 1 K. y
de ig Sauts Crique ела эы saut Be

1996, Grenand 1277 Ү); Piste de St. Elie ‚ 6 Now
1255 Riera 415 10055
12. Bot. Jahrb.

Dracontium longipes Engl.,
Syst. 37: 122. 1905. TYPE: Brazil. Acre: Be-
lem at ae Miry, 8°S, 72%59'W, Sep. 1901.
E. Ule 5781 (holotype, B!; isotype, B!). Figure
15.

Tuber hemispherical, 10-15 em diam., 6-10 em
thick, flat or slightly sunken above, rounded and
whitish to brownish below, 10-25 cm below ground
level; tubercles abundant, borne around the pe-
riphery of tuber; roots strong; cataphylls 1 to 3, 10—
25 X 1-3 cm, light brown, reaching or surpassing
ground level. Leaves solitary; petioles 1-2 m long
above ground, 3—4 cm diam. at midpoint, dark
green, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern, usu-
ally smooth in upper half and with irregular pro-
tuberances in lower half; juvenile blade sagittate,
or sagittately lobed; mature blades spreading hori-
zontally, 1-1.2 m diam., papyraceous, sometimes
fenestrate, never variegated, sometimes with abun-
dant raphide cells, semiglossy and dark green
above, matte and medium green below; middle di-
vision 3 times or more trichotomously branched,
0.6-0.75 X 0.5-0.6 cm, with terminal subdivision
consisting of 3 sections, with each basal subdivi-
sion consisting of many segments; lateral divisions
3 times or more dichotomously branched, 0.45-0.7
X 0.5-0.6 ст, with terminal subdivision consisting
of 2 sections, with basal subdivision consisting of
many segments; terminal and subterminal sections

Volume 91, Number 4 Zhu & Croat 635
2004 Revision of Dracontium

0.6 cm

Figure 15. A-D, Dracontium longipes. —A. Inflorescence with the lower portion cut away to expose the spadix.
—B. Live plant with portion of leaf and infructescence with persiste nt spathe. —C. Lower portion of spathe cut open

pa
showing close-up of spadix (Croat 95460). —D. Seeds in side view (Croat 72368).

Annals of the
Missouri Botanical Garden

free; leaf segments often entire, broadly oblanceo-
ate, more than 5 em wide on each side of the major
each

—

ribs, ovate, mostly free from each other ii
division, often with contrastingly smaller rounded
or triangular segments alternating with larger seg-
ments; apices caudate; ultimate segments 10-15 cm
long, confluent. with penultimate segments; other
segments 9-16 cm long: penultimate segments free
from subterminal sections; medial segments free
from basal subdivisions; basal segments present,
free from each other; rachises patterned similar to
petiole but in much paler shades, sometimes with
spiny projections; tertiary veins obscure above and
weakly raised below; bracteoles 1 or 2, 10-25 X l-
2 em, dark brown,
than the peduncle, confined at the base. /nflores-
cence solitary, appearing before new leaf; peduncle
60-100 em long above ground, 1-2 cm diam. at

midpoint, less than half as long as the petiole, mot-

the longest one much shorter

tled similar to petiole but deeper in color, dark
green, ines or with irregular protuberances and
spiny projections; spathe 23-25 cm long, 5-6 cm
wide, eymbiform, cucullate, erect or slightly arch-
ing, apex acuminate; inner surface velvety, maroon,
with translucent area obvious, 2—4 cm high, as long
as spadix; outer surface violet-purple tinged green,
matte; margins entire, broadly overlapping in the
lower half; veins conspicuous inside, conspicuously
darker or paler than the spathe, brownish; spadix
ipu Pope: cylindric, light brown or purple.
-3.5 0.5-0.7 em at anthesis, never with ap-
айе Н at apex: stipe 0.5-1 cm long, 0.4-0.5 cm
diam. at anthesis. Flower tepals 4 to 6, 1-1.5 mm
long, 0.5-1 mm wide, light brown; stamens 7 or 8:
filaments 0.5 mm long: anthers 0.5 mm long. hid-
den; ovary bilocular, pale green: stigma 2- or 3-
lobed; style 1—1.5 mm long above tepals, brownish
purple, persistent. Infructescence with spadix 4:
em long, 2-2.5 em diam. in fruit, berries l-se eded,
0.4-0.6 em diam., 0.5-0.8 em thick, obliquely ob-
ovoid, apically rounded; berries medium
green; mature berries color unknown, without red-
dish dots and raphide cells, 0.6-0.7
diam., reniform, reddish brown, laterally depressed:

dorsal ridges obvious, 3, continuous, monomorphic,

young

seeds cm

more than 1 mm thick, 0.5 mm high, smooth on

both sides (sometimes with a few warts).
Phenology. Flowering from May to September:
mature fruits are known only in August.
Distribution and habitat. Dracontium longipes
is limited to the area near the border of Acre, Bra-
zil. and Madre de Dios, Peru. It occurs in Tropical
moist forest (V-mf) and Premontane wet forest (P-wf)

life zones (Holdridge et al., 1971), at elevations of
150 m.

Discussion. Dracontium longipes is easily con-
fused vegetatively with D. plowmanii and D. spru-
ceanum, but is distinguished from those species by
having a cymbiform rather than an erect or arching
spathe. Dracontium plowmanii also differs from D.
longipes in having a spathe with undulate or lobed
margins and small seeds with a single continuous
ridge. In contrast, the spathe of D. longipes has
straight margins and the seeds have three obvious
dorsal ridges. Dracontium spruceanum differs in
having seeds with more than three dorsal ridges.
BRAZIL. Acre: IN-

1 specimens examined.
k

CRA at ca. 4 km S of main rd. Cruzeiro do Sul to Rio
p Croat 62349 (MO); Rio is Miry, Ule 5272 (B):
Vista Alegre, Rio Jurua Miry, Croat. 85460 n Rio
ну to Miri rim at Porangaba, et al. 132 NY):

T
Santa Rosa, Rio Purus, Daly el » 10000 Dus Г E RU.
ios: Manu Park, Cocha Cashu, Río Manu,
MO, QCA), Núñez et al. 14420 (MO)

Ma dre de Di
Foster 6978 (F,
13. Dracontium margaretae Bogner, Aroideana
1: 87. figs. 1-6. 1981. TYPE: Brazil. Mato
Grosso do Sul Panu Indigena do Xingu,
Posto Leonardo, 23 Nov. 1973, M. Emmerich
4053 (holotype, RI; isotype, M!). Figure 16.

Dracontium 6 S. Bunting & 9 Phytologia 64:
YPE:

164. 1988. Syn. nov. TYPE: Venezuela. Apure:
Ac a, у ‚ Rómulo Gallegos, Rio ا‎ ack poco
arriba de El Porvenir, en las cercanías del Hato San

varios ре queños ae ntos Pumé
Mangos, Las Maravillas y Las
Campanas, 6° 18-5 52˙N. 68°45— 18'W, 80 m, 10 July
1986, T. els Sua К G. Gragson 13 (holotype, US;
. МҮК MCA not seen, UCV not

| JOS
nol seen,

Tuber hemispherical or irregular-shaped, 10—12
em diam., 8-10 em thick, flat or slightly sunken
above. rounded or flat and whitish to light brown
10-15 em below ground level; tubercles
abundant, cylindrically elongated, 0.5-0.8 cm
1—2.5 em long, borne around the periphery
Roots whitish sometimes

below,

diam.,
and the side of tuber.
tinged brown, to 3.5 mm diam.: cataphylls 1 or 2,
10—30 em long, 2—4 em wide, pinkish or reddish
brown, 5—15 em long above ground. Leaves solitary
or sometimes 2 or more per tuber; petioles 0.3—0.9
m long above ground, 2-3 em diam. at midpoint,
light green (in upper half) or brown-green (in lower
half), weakly mottled, smooth (often); juvenile blade
linear or trifid; mature blade ascending to 45° to
the aide 0.5— | diam., thinly coriaceous,
never fe bien never variegated, without raph-
ide cells or dark markings, semiglossy and medium

green above, semiglossy and medium green below:

Volume 91, Number 4 Zhu & Croat 637
2004 Revision of Dracontium

0.5 cm

Figure 16. A-D, Dracontium margaretae. —A. Tuber, petioles, cataphylls, and an 5 e (Catharino 1832).
—B. Potted plant with tuber bearing tubercles, a fully formed leaf. and an opening leaf (G. Zhu 1533). —C. Ti iber

with infructescence, type specimen (Emmerich 4053). —D. Seed in side view (T. G. вум 4).

638

Annals of the
Missouri Botanical Garden

middle division twice trichotomously branched, 37—
45 X 30-40 cm,

sisting of three sections, with each basal subdivi-

with terminal subdivision con-

sion consisting of many segments; lateral divisions
35-45 X 30-40

cm, with terminal subdivision consisting of 2 sec-

twice dichotomously branched,

tions, with basal subdivision consisting of many
segments; terminal and subterminal sections free,
each usually consisting of a single segment; leaf
segments often entire, linear, less than 1 em wide
on each side of the major ribs, linear, mostly free
from each other in each division, without contrast-
ingly smaller rounded or triangular segments; api-
ces acuminate; ultimate segments 10-20 ст long,
free from penultimate segments; other segments
10-30 cm long; penultimate segments free from
subterminal sections; medial segments free from
basal subdivisions; basal segments absent, free
from each other; rachises patterned distinct from
petiole, pale green, smooth; tertiary veins conspic-
uous above and weakly raised below; bracteoles 2
or 3, 6-25 cm long, 1-3 em wide, dark brown or
pinkish, the longest one shorter than the peduncle,
reaching the spathe. /nflorescence solitary, appear-
ing after new leaf; peduncle 3-10 cm long above
ground, 0.5-1 ст diam. at midpoint, often almost
completely subterranean (or under water), scarcely
mottled, whitish tinged pink, smooth; spathe 4—8
cm long, 1-2.5 cm wide, cymbiform, cucullate,
arching 90° (or more), apex acuminate; inner sur-
face covered with dense, translucent scales to 1 mm
long, olive-brown, with translucent area obscure;
outer surface maroon tinged brown, matte; margins
entire, slightly overlapping at the base; veins ob-

scure inside and raised outside, conspicuously
darker or paler than the spathe; oe exposed,
stipitate, cylindric, brown, 1.3-2 X 0.6-1 ст at

anthesis, often with several appendages at apex;
stipe 0.4—0.5 X 0.3-0.4 ст at anthesis. Flower te-
pals 5 to 6, 1-2 mm long, 0.5-1 mm wide, brownish
purple; stamens 6; filaments 1-2 mm long; anthers
0.5 mm long. completely exserted; ovary bilocular,
pale green; stigma 2-lobed; style 1-2 mm long
above tepals, brownish purple, persistent. /nfruc-
tescence with spadix 2-4 X 1.5-2.5 cm in fruit:
berries 2- or 3-seeded, 0.5-0.9 х 0.7-0.8 cm, glo-
bose or subglobose, 3- to 6-angular, apically round-
ed or subtruncate, drying ca. 7 mm thick, 2- or 3-
lobed; young berries medium green; mature berries
reddish or purplish red,

with abundant. raphide
seeds 0.4-0.6 cm di i

diam., reniform, light
2.2-2.3 cm thick;

sparsely beset with irregular warts dorsally, dorsal

cells;

brown, laterally depressed,

ridges obscure.

Phenology. Flowering from May to November;
mature fruits are known only in May.

Distribution and habitat. Dracontium margar-
etae is known only from a few localities in Brazil
(Mato Grosso do Sul), Paraguay, and Venezuela
(Apure and Guárico). It occurs in seasonal swamps
in the Tropical moist forest (T-mf) life zone (Hold-
1971), at elevations of ca. 100 m
Dracontium margaretae is an atyp-

ridge et al.,

Discussion.
ical member of the genus, recognized by its linear
blade segments and by occurring in seasonally
swampy habitats. Other distinguishing features in-
clude the linear or trifid juvenile leaf blades and
tubercles borne at the apex and sides of the tuber.
It is confused with no other species. This species
grows well as an aquatic in cultivation.

The species described under the name Dracon-
tium lineare G. S. Bunting & Tillett (Bunting, 1988)
is identical to D. margaretae; therefore, the former
name 1s treated as a synonym of the latter.

Additional specim xamined. BRAZIL. Palmas, Es-
trada para Toes 'antinia, a ome 97 (UB). Mato Grosso
do Sul: Parque Indigena do Xingu, Posto Leonardo,
Emmerich 4598 (K, M); Puerto Joáo André- prea
ca. 7 km before Brasilándia, Catharino et al. 5Р).
РАКАС eo s Laguna, Est. Keicus, RR 10960
G, MO). VENEZUELA. Apure: Dist. Achaguas у Ró-
mulo CUM Río Capanaparo, El. Porvenir, Gragson &
Gragson 4 (US), 13 (MYF, VEN). Guárico: Santa Rita
near r the rd. to Calirita. Susach 251 (VEN), Trujillo 12633
(

—

Cultivated plants. Brazil. Mato Grosso do Sul, vouch-
ered as Catharino 1832, cult. at Jardim Botánico de Sao
Paulo, б. Zhu 1533 (MO, SP).

14. Dracontium nivosum (Lem.) С. Zhu, World
Checklist & Bibliogr. Araceae, 301. 2002.
Amorphophallus nivosus Lem., Ill. Hort. 12: 1,
fig. 424. 1865. TYPE: figure 424 in III. Hort.
12: 1865 (lectotype, designated here). Figure
17.

маа papillosus hort. ex Rafarin, Rev. Hortic.

6, fig. 65. 1871. TYPE: figure 65 in Rev. Hor-

| eis 477 , 1871 (lectotype, designated here).

Tuber үү or rounded, 6-12 cm diam.,
4—8 cm thick, ove, rounded and white to
brown below, dip cm below ground level; tuber-
cles few, rounded, 0.8-1.5 cm diam., borne around
the periphery of tuber, roots white, 2-3 mm diam.;
cataphylls 1 to 3, 9-28 X 2-3 cm, light brown,
reaching or surpassing ground level. Leaves solitary;
petioles 1-2 m long above ground, 2.5—3 cm diam.
at midpoint, dark green, contrastingly mottled with
dirty white or pale green blotches and forming a
reptilian pattern, usually smooth in upper half and
with irregular protuberances in lower half; juvenile

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

LETRA

ға
в

í

Figure 17.

A-D, Dracontium nivosum. —A. Cultivated plant at John Banta’s nursery. Immature infructescence. —B. Cultivated plant at John Banta’s nursery. Flowering plant at

(Huber 3667). Seeds in side view. —D. (Hetterscheid AR-017). Inflorescence with spathe cut open to expose spadix. Photo by W. Hetterscheid.

C:

anthesis.

640

Annals of the
Missouri Botanical Garden

blade sagittate, or sagittately lobed; mature blade
spreading horizontally, 0.8—1 m diam., often thinly
coriaceous, rarely fenestrate, sometimes variegated
(along the veins), without raphide cells or dark
markings, matte and medium green above, matte
and pale green below: middle division twice tri-
chotomously branched (often), 30-45 X 20-40 cm,
with terminal subdivision consisting of 3 sections,
with each basal subdivision consisting of many seg-
ments; lateral divisions
branched, 28—45 X 30—45 cm, with terminal sub-

division consisting of 2 sections, with basal sub-

twice dichotomously

division consisting of many segments; terminal and
subterminal sections free, each consisting of many
segments; more than 5 cm
wide on each side of the major ribs, ovate or ob-

broadly oblanceolate,

lanceolate, mostly free from each other in each di-
vision, often with contrastingly smaller rounded or
triangular segments alternating with larger seg-
ments; apices acuminate; ultimate segments 6—8 cm
long, often confluent with penultimate segments:
other segments 5—12 cm long; penultimate seg-
ments free from subterminal sections; medial seg-
ments free from basal subdivisions; basal segments
present, free from each other; rachises patterned
similar to petiole but in much paler shades, with
spiny projections; tertiary veins obscure above, or
conspicuous below; bracteoles 3 or 4, 2-28 X 1-2
cm wide, light brown, the longest one + as long as
the peduncle, reaching the spathe. Inflorescence
solitary, appearing before new leaf; peduncle 0—2
cm long above ground, 1-1.5 em diam. at midpoint,
often almost completely subterranean, scarcely
mottled, whitish tinged pink, smooth; spathe 28-35
х 6-10 cm, cymbiform, cucullate, arching to 45°,
apex acuminate; inner surface semiglossy, maroon,
with translucent area obscure; outer surface ma—
roon, matte; margins entire, broadly overlapping in
the lower half; veins obscure inside and raised out-
side, similar to the spathe in color: spadix hidden,
stipitate, cylindric, purple or brown-purple, (3-)5—
6.5 cm long, 1.2-1.5 em diam. at anthesis, never
with appendages at apex: stipe 0.6-1.2 cm long,
0.5-1 ст diam. at anthesis. Flower tepals 5 to 8.
2.5-3 mm long, 1-2 mm wide, purple; stamens 6
to 8; filaments 2-2.5 mm long; anthers 0.5-1 mm
long, slightly exserted; ovary 3-locular; stigma 3-
lobed; style 4—5.5 mm long above tepals, purple.
Infructescence with spadix 12-18. em
em diam. in fruit; berries 3- or 4-seeded
2-seeded, 0.8-1 cm diam., 0.8-1 cm
thick, subglobose, 3- to O-angular, apically trun-

persistent.
long, 3-3.5

or sometimes

cate; mature berries orange (tinged red), with abun-
dant raphide cells; seeds 0.5—0.7 em diam.,
form or

reni-

rounded, light brown, laterally raised:

dorsal ridges obvious, 3, continuous, less than 0.5
mm thick, 0.1 mm high, finely decorated with small
cells on both sides.
Phenology. Flowering May
fruits from December to March
Distribution and habitat. Dracontium nivosum
is endemic to Pará and Maranhao, Brazil. It occurs
in Tropical moist forest (T-mf) and Tropical wet forest
(T-wf) life zones (Holdridge et al., 1971) at eleva-
tions of 30 to 150 m.
"Tajá de cobra" (Black 47-2084,
z); “jararaca-taja” (Schott, 1865: 73).
Discussion.

July; mature

Local names.

z

“~

ч
—

Dracontium nivosum is character-
ized by its subterranean peduncle with a strongly
hooded and cymbiform spathe, a spathe much larg-
er than that of any other member of the genus pos-
sessing subterranean peduncles. Other species with
peduncles at least sometimes subterranean such as
D. amazonense, D. bogneri, D. dubium, D. grayu-
mianum, D. polyphyllum, D. prancei, D. purdiean-
um, D. soconuscum, and D. ulei have spathes only
3-15(18) em long, whereas the spathe is 28-35 cm
long for D. nivosum. Other species that, like D.
nivosum, have the spadix hidden at anthesis owing
to the broadly overlapping spathe base include D.
amazonense, D. bogneri, D. prancei, and D. ulei, but
none of them have ranges overlapping that of D.
nivosum.

Common names attributed to snakes obviously
refer to the reptilian pattern exhibited by the pet-
ioles. Perhaps for the same reason many species of

Dracontium are us

ed by native populations for
snakebite remedies (Croat, 1994). This species is
known in cultivation at the Instituto Agronomico do
Norte (IAN) at Belém, Pará State, Brazil. A plant
of the species, collected from Santarem, Brazil,
flowered in John Banta's nursery in Florida in 1993.

Since no type was chosen for Amorphophallus ni-
vosus Lem., the only plate from the protologue (Ш.
Hort. 12: 1, fig. 424. 1865)

lectotype for the name. Two figures of this species

is designated here as a

appeared earlier before its publication under the
name D. polyphyllum (Bot. Reg. 9: fig. 700 A&B,
1323)

Apparently based on a cultivated plant, another
name, 5 papillosus hort. ex Rafarin
(Rev. Hortic. 43: 476, 1871), was published for the
same species. In the protologue of A. papillosus, no

J

type was designated and one illustration (fig. 65 in
Rev. Hortic. 43: 477, 1871) was included with a
caption mistakenly noted as A. nivosus. For the in-
tegrity of nomenclatural citation, the illustration
(fig. 65 in Rev. Hortic. 43: 477, 1871) is designated

here as a lectotype for the name A. papillosus.

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

Dracontium nivosum was previously noted (as
nomen nudum) to occur in Peru (Vásquez et al.,

2002 [2003 .

Additional specimens examined. BRAZIL. Maran-
130: Monção, P. I. Guajá, Río Turiaçu, Guajá Indianas,
Balée 3476 ( ará: ÓN bei Santarem,”

June 1927, Ginzberger 3109 (WU); Barcarena, Itupanema,

Gély 234 (MG): Mpo. Tucuruí, Río 'antins, 1-5 km from

Represa Tua иги, Plow nan е 1 95 ев de Cupari,
Ma-

Ingatuba capoeira, Blac 1 RB); BR-423,
chiel & ЖКК 534 С): T igia, Campina do ИТ Black
16814 (IAN): Paraenfis, 1911, Martius 282 : Belém-
Sao Caetano, km 12, Lobato et al. 60 (MG).
Cultivated plants. Brazil. Para, Belém, Museu Par

‚ Botanical Garden, May 1901, Huber
ask lituto Agronomico do Ko (IAN) at
Belém, ш. 19 1 IAN. MG), Pires 6594 (IAN

15. Dracontium peruvianum G. Zhu & Croat.
TYPE: Peru. Loreto: Maynas. Allpa-
huayo, 4^10'S, 73°30'W, 150-180 m. 4 Dec.
1990, K. Vásquez & N. Jaramillo 15226 (ho-
lotype, MO). Figure 18.

5р. nov.

Herba usque pus quam 6 m alta; petiolus 2-6 m lon-

gus; lamina 0.6-1 m longa, 0.6-0.9 m lata: pedune ‘ulus
60-115 em ane 1 .5—6 cm diam.; spatha (25)30-50 cm
longa, 6-10 cm lata; extus rige o intus ve-
lutina, purpurea; spadix 8-10.5 cm longi 1-1.3 en
diam.; baccae 0.7—1 cm diam.: semina a ‘a, 0.7-1 ст
diam

Tuber hemispherical, 10-30 em diam.. 8—15 ст

rounded and white to brown be-
15-45 cm below ground level: tubercles few.

thick, flat above,
low,
rounded or cylindrically elongated, borne around
the periphery of tuber; roots white, to 0.4 mm
diam. cataphylls 1 or 2, 10—50 X 2.54 cm. reach-
ing or surpassing ground level. Leaves solitary: pet-
ioles 2-6 m long above ground, 3.6-5 em diam. a

—

midpoint, dark green (paler toward the apex), con-
trastingly mottled with dirty white or pale green
blotches and forming a reptilian pattern, usually
with spiny projections (especially in upper half or
at the apex): juvenile blade sagittate, or sagittately
lobed: mature blade spreading horizontally. 1.2—2
m diam., thinly coriaceous, rarely fenestrate or
the
lacking raphide

sometimes fenestrate throughout blade (in
young leaves), never variegated,

cells or dark markings, semiglossy and dark green
middle di-
60—100 x
60-90 cm, with terminal subdivision never divided

above, matte and medium green below:
vision twice trichotomously branched,
into sections, with each basal subdivision consist-
lateral divisions twice di-
55-05 X 55-90 cm.

terminal subdivision consisting of 2 sections, with

ing of many segments:

chotomously branched. with

basal subdivision consisting of many segments: ter-

minal and subterminal sections confluent, each

consisting of many segments; broadly oblanceolate,
more than 5 cm wide on each side of the major
ribs, oblanceolate, at least some of the basal seg-
ments free from each other, without contrastingly
smaller rounded or triangular segments; apices
acute or acuminate; ultimate segments 20-27 cm
long, often confluent with penultimate segments;
other segments 10—15 cm long; penultimate seg-
ments free from subterminal sections; medial seg-
ments free from basal subdivisions; basal segments
present, free from each other; rachises patterned
similar to petiole but in much paler shades, smooth;

tertiary veins obscure above and weakly raised be-

—

low: bracteoles 1, 15-50 cm long. 2—4 em wide.
light brown, the longest one much shorter than the
peduncle, confined at the base of the peduncle. /n-
florescence solitary, appearing before new leaf; pe-
duncle 60-115 X 1.5-6 cm diam. at midpoint. less
than half as long as the petiole, mottled similar to
petiole but deeper in color, brownish green, with
irregular protuberances in lower half and spiny pro-
jections (in upper half, especially at the apex):
spathe (25-)30-50 X 6-10 cm,

cucullate, erect or slightly arching, apex acuminate;

cymbiform, non-
inner surface semiglossy, maroon, with translucent
area obvious, 5-8 cm high, shorter than spadix:
outer surface maroon tinged brown, matte; margins
entire, slightly overlapping at the base: veins ob-
inside and raised outside,

scure conspicuously

darker or paler than the spathe; spadix hidden,
stipitate, cylindric, brown or brown-purple. 8—10.5
X 1-1.3 cm at anthesis, never with appendages at
apex: stipe 0.5-2 X 0.5—1 ст at anthesis. Flower
tepals 5 to 7, 1-2 X

brown-purple; stamens 7 to 11; filaments 1-1.5 mm

-2.5 mm, light brown or
long: anthers 0.5 mm long, hidden; ovary 3-locular,
pale green; stigma 2- or 3-lobed: style 1—1.5 mm

long above tepals, brownish purple. persistent

~

TE
x 2.8-3 cm

0.5-1 em diam.,

not. Infructescence with spadix 23-35

fruit: berries 1- to 3-seeded,
0.7-1 em thick, obliquely obovoid or globose, api-
cally rounded or subtruncate; young berries medi-
um green; mature berries orange, without reddish
0.7-1

rounded, dark brown, laterally raised: dorsal ridges

dots and raphide cells: seeds em diam.
obvious, 3. continuous or rarely strongly interrupt-
ed, with the central ridge contrastingly raised, more
mm thick,

than | 1-2 mm high. smooth on both

sides.
Phenology. Flowering April to November; ma-
ture fruits July to March, with a peak in December.
Distribution and habitat. — Dracontium peruvian-
um is known only from Amazonian Peru and Brazil.
It occurs in Tropical moist forest (V-mf). Premontane

642 Annals of the
Missouri Botanical Garden

Figure 18. A-D, Dracontium peruvianum. —A. Inflorescence in Ucayali Department, Peru. Photo W. Sta
Flowering plant in Parque Nacional Alexander von Humboldt, near Puc salpa, Ucayali Department, Peru. Photo by A.
Salazar. —C. Infructescence with persistent spathe type specimen (Vásquez & Jaramillo 15226). —D. Seeds in lateral

view (Gentry & Daly 18798).

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

643

moist forest (P-mf), and Tropical montane moist for-
t (TM-mf) life zones (Holdridge et al., 1971), at
elevations of 180 to 900 m

Local names. “Jergón sacha” (Plowman &
Schunke 11536, MO).

Discussion. Dracontium peruvianum has the
longest leaves of any species in the genus, up to 6
m long. The inflorescences of this species are su-
perficially similar to those of D. pittieri, but are
distinct by the more elongate fruiting spadix (to 23—
35 em long vs. 10—20 cm long for D. pittieri). more
strongly ridged seeds (vs. less ridging in D. pittieri),
and basal leaf segments that usually are free from
the rachis.

In having such a long peduncle D. peruvianum
is similar to D. asperispathum, D. croatii, D. gran-
dispathum, D. longipes, D. plowmanii, and D. spru-
ceanum, but only D. croatii, D. longipes, and D.
pittieri also have a cymbiform spathe that is not
differentiated into a proximal tube portion and a
distal lamina. Dracontium croatii and D. pittieri dif-
fer in having the spathe obtuse at the apex (vs.
acuminate for D. peruvianum and D. longipes). Dra-
contium longipes differs from D. peruvianum in hav-
ing a much shorter infructescence (only 4—5 ст
long vs. 23-35 cm long for D. peruvianum).

Paratypes. BRAZIL. Amazonas: Rio Juruá basin,
near mouth of Rio Embira (tributary of Rio Tarauaca).
Krukoff 4987 (GH, NY). PERU. Huánuco: Pachitea,
Honoria, Río Pachitea, Schunke- 1055 1775 (F): Tingo Ma-
ría, Gentry & Daly 18798 (F, MO). Loreto: Río Amazon-
as, Isla de Iquitos, Rimachi 5304 риш Nauta, Vásquez
& Jaramillo 8562 (MO); Fernando I
shiyacu, Grández et al. 2629 (MO ` Rimachi 1043 (IBE);
Iquitos, I. Williams 7916 (F); Rio аза just below mouth
of Rfo Ucayali, Gentry et al. 30026 (MO); San Antonio,
ya. Vásquez & Jaramillo 3598 (MO); Río Ucayali,
Santa Rosa, 5 : E ee NCSU E Sta-

—

ebrada Tam-

=

Amazon River, L. Williams 1561 (F). Pas
ley, [sc 5 уезде PEPP Project 3 Salick 7370

(MO). San Martin: 12 km W of Tocache Nuevo, Gentry
et al. Pots MO). Trae Yurimaguas, km 40, trail to
Río Tiriyacu = ashiyacu, :

(МО); Tocache oe Tocac
23, Rio Cafiuto, Plowman & Schunke 11536 (F, MO, SEL);

mas Convento, Tarapoto-Yurimaguas, km 68, Alcorn &
ariscal Caceres, Dtto. Tocache Nuevo,
Schunke 1 (MO): Puerto
UCLA); Yorongos-
der — al. 16538 (AAU,

, CAS, К, MEXU, MO, "US, USM

ooi plants. Peru. Hu а National Park Бе-
tween Pucallpa and jr María, collected by Angel Sa-
lazar, cult. at MBG, J. B. Croat 53539 (MO).

16. Dracontium pittieri Engl., Anales Inst. Fis.-
Geogr. Nac. Costa Rica 9: 209. 1896. TYPE:
Costa Rica. Puntarenas: Río Naranjo, 200 m,

H. Pittier & A. Tonduz 7515 (lectotype, des-
ignated here, CR!; isotypes, B!, BR!). Figure
19

6—8 cm
thick, flat above, rounded and white to brown be-

Tuber hemispherical, 14-20 cm diam.,

low, 20-40 cm below ground level; tubercles abun-

dant. irregular-shaped, 0.3-1.5 cm long. borne
around the periphery of tuber; roots white, to 3 mm
cataphylls З to 5. 4—40 х 4-7 cm, light

brown, reaching or surpassing ground level. Leaves

diam.;

solitary; petioles 1.84 m long above ground, 5-8
em diam. at midpoint, dark green or brownish
green, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern,
smooth or usually with spiny projections; juvenile
blade sagittate, or sagittately lobed; mature blade
1.2-2 m diam.,

ceous or thinly coriaceous, rarely fenestrate,

spreading horizontally, subcoria-
never
variegated, with abundant raphide cells (some-

times), glossy and dark green above, semiglossy
and medium green below; middle division 3 or more
times trichotomously branched, 80-120 х 50-100
cm, with terminal subdivision consisting of 3 sec-
tions, with each basal subdivision consisting of
many segments; lateral divisions 3 or more times
70-120 Xx 55-90 cm,

with terminal subdivision consisting of 2 sections,

dichotomously branched,

with basal subdivision consisting of many seg-
ments; terminal and subterminal sections confluent,
each consisting of many segments; leaf segments
bilobed or trilobed, oblanceolate,

than 5 cm wide on each side of the major ribs,

broadly more
oblanceolate or lanceolate-ovate or triangular,
mostly confluent with each other in each division,
often with contrastingly smaller rounded or trian-
gular segments alternating with larger segments;
apices narrowly acuminate, or caudate; ultimate
segments 10—20 cm long, confluent with penulti-
male segments; other segments 10—30 cm long;
penultimate segments confluent with the subtermi-
nal sections; medial segments confluent with the
basal subdivisions; basal segments present, conflu-
ent with each other; rachises patterned distinct
from petiole, pale green, smooth; tertiary veins ob-
scure above, or conspicuous below; bracteoles 3 or
4. 4—40 cm long, 5—7 cm wide, pinkish, the longest
one much shorter than the peduncle, confined. at
the base. Inflorescence solitary, appearing before
new leaf; peduncle 150—250 cm
diam. at midpoint, more than half as long

m long above ground,

cm
as the petiole, mottled similar to petiole but deeper
in color, dark green, smooth or with irregular pro-
tuberances; spathe 30—50(70) em long, 8-12 em

wide, cymbiform, non-cucullate, erect or slightly

Annals
мо 8 Garden

1 —

D. Dracontium pittieri. A-C,

Close-up of spat

1e with one side
ew

(Burger 58 Seeds in side vi

(Croat & Hannon 79217). —A. Habit of flowering plant with Dylan
removed to expose spadix. С. Infructescence with premature berries.

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

arching, apex obtuse; inner surface semiglossy, ma-
roon or olive-brown or red-purple, with translucent
area obvious, (5) 10-17 em high, 1.5 to 3 times lon-
ger than spadix: outer surface maroon, matte; mar-
gins entire, hardly overlapping at the base: veins
obscure inside or raised outside, similar to the
spathe in color: spadix exposed, sessile, cylindric,
brown-purple (tinged green) or purple, 4-9 X l-
1.5 em at anthesis, never with appendages at apex.
Flower tepals (4)5 or 6(9), 3—4 mm long, 1-1.5 mm
wide, brownish purple or dark purple: stamens 12
to 15: filaments 2-3 mm long: anthers 1 mm long.
slightly exserted; ovary bilocular, whitish; stigma
(2)3(4)-lobed; style 3—4 mm long above tepals, pur-
ple, persistent. /nfructescence with spadix 10-20 cm
long, 3—4 em diam. in fruit; berries 2-seeded, 0.6—
3- to
6-angular, apically truncate; young berries medium

1.2 em diam., 0.9-1.3 em long, subglobose,
green: mature berries orange, with abundant raph-
ide cells: seeds 0.9-1.1 em diam., reniform or tri-
angular, light brown, laterally flattened: dorsal ridg-
es obvious, I. continuous, more than 1 mm thick,
0.5-1 mm high, warty along both sides, appearing
as strongly reduced lateral ridges.

Phenology. Flowering from May to November:
one inflorescence was also collected in February:
mature fruits in November and February.

Distribution and habitat. Dracontium pittieri is
endemic to the Pacific slope in Puntarenas Prov-
ince and adjacent San José Province in Costa Rica.
lt occurs in Tropical moist forest (T-mf) and Pre-
montane moist forest (P-mf) and Tropical wet forest
and transition forest to Premontane wet forest life
1971).

along river banks, roadsides, secondary growth, and

zones (Holdridge et al., It is often found
other disturbed areas, at elevations of 30 to 1000
m.
Discussion. | Dracontium pittieri is characterized
by having the longest peduncles in the genus. It is
easily confused with D. gigas in sterile condition,
but differs strikingly in inflorescence morphology
(see also discussion of D. gigas). Dracontium gigas
has a large spathe and a short peduncle, which is
always less than twice as long as the spathe. where-
as D. pittieri has a much longer peduncle, 5 to 8
times longer than the spathe. The spathe of D. gi-
gas is more or less hooded at the apex. with the
margins broadly overlapping and completely cov-
ering the spadix. The spathe of D. pittieri is open
at the apex with the margins scarcely overlapping.
such that the spadix is exposed. The translucent
area at the base of the inner spathe surface extends
much higher than the spadix in D. pittieri, while it
never exceeds the height of the spadix in D. gigas.

Aside from the fact that they are widely sepa-
rated geographically. D. pittieri could also easily
confused with D. peruvianum; they differ, however,
in the features of infructescences, seeds, and leaf
A few

plants of this species have been brought into cul-

blades (see discussion of D. peruvianum).

tivation in the United States, but no report of flow-
ering is known. Several plants of D. pittieri are
known from John Banta’s Nursery (Alva, Florida).

In the protologue, two specimens, Pittier & Ton-
duz 7515 and Pittier 11985, were cited without in-
1896).
one of them needs to be designated as the holotype.
The Pittier & Tonduz 7515 collection has three du-
plicates that are deposited in three different her-

dication of a holotype (Engler, Therefore,

baria (B. BR. CR) and are in much better condition
than the unicate Pittier 11985; therefore. the former
collection is designated here as lectotype for the
name D. pittieri. A description of this species was
published at a later date (Engler, 1905)

Additional specimens examined. POL RICA. Pun-
tarenas: Boca Culebra, Pittier 11985 ; Fila de Cal,
betw. San Vito & Ciudad de ily, н р et E 6046 (MO):
Cantón de Osa, 2.5 mi. SW of Rincón, Croat & Grayum
59844 (CM, M0). a 1646 (MO); Fila Retinto. cer-
ros N Palmar Norte, Hammel 17713 (CR):

mado, Rincón, Marín 285 (CR, MO). Quesada 259 (CR,
ru МО); above Palmar Norte, Allen (КАР, MO.
O). po 35104 (CM, F. MO); vie. 1 1 1 el

al 15204 (MO);
Burger & Stolze 5551 (F,
5 ig а Herrera 4529 (MO)

5 km W of Rincón de Osa W of airfield.
Y); Quebrada Orito & Quebra-
Corcovado Nat. Park.

‚ Liesner 2867 p^ МО); Los Patos Forest, Aernan
£ "Phillips 648A por gp os Patos, Cerro de Oro, Aguilar
& Guzmán 2849 Sabanillas de Limon-

CR); Coto Brus,
SA,

Me, Alpin 85. 34 (SEL);
JE of Santa Marta, Gómez 22935 (CM,
1085 i 25

Gol fito- а si de Gene eral, Kress 7 76

Juena, 4 ve . airport. Piste 2017 (MO): Rio Nar-
anjo, near Londres & Villa Nueva. Burger et al. 12260
К); vic. of Bosco Aguabuena, Croat & Hannon

79217 (MO, NY. Wi " à Golfito, PN Corcovado, Angulo 273
(INB, MO). San José: R. Ocampo S. 2573 (CR): La Can-
greja, Cerros de Puriscal, Santa Rosa de Puriscal, Morales
546 (CR); Playa, Dominical/Baru/Tinamastes, along rd. to
San Isidro del General, Burger & Baker 10131 (F, MO)

17. Dracontium plowmanii G. Zhu « Croat, sp.
nov. PYPE: Peru. Cuzco: Раис 'artambo, Pilco-
pata, Villa Carmen, 720 m, 7 Feb. 1975, J.
Plowman & W. Davis 5054 dane GH':
isotype, US)). Figures ТА. 20

Petiolus 1-2 m longus; lamina 45-55 cm longa, 40-55

m latis; pedunculus 29.5-70 em longus, 1-2 em diam.;
eee: 3-20 cm longa, 2.5-3.5 em lata, cucullata vel
non cucullata basi; extus polit, purpure " m velu-
tina, purpurea; spadix 3—4.9 cm longus. —1.2 cm

е

Annals of the
Missouri Botanical Garden

№, $

Figure 20. A-D, Dracontium дери. Photos т C by P. Schmidt. —A. (Selby ۰ пз 76-575). Inflorescence
(С. Zhu 1446). B, C, (Selby Garder 21). —B. Spathe in side view with petiole. —C. Leaves of potted plant. —
D. Seeds in lateral view. Note: eac h line c on left of 3985 represents 1 mm (Cornejo о.

Volume 91, Number 4
2004

Zhu & Croat 647

Revision of Dracontium

diam.; tepala 4—6; baccae 0.7—1 ст diam.; semina brun-

neola, 0.1—0.6 em diam.

Tuber hemispherical, 10-20 cm diam., 6-9 cm
thick, flat above, rounded and white to brown be-
low. 5-18 cm below ground level; tubercles few,
rounded or cylindrically elongated, 0.5-0.8 cm
diam., 0.8-1 em long, borne around the dr
of tuber; roots white, strong; cataphylls 2 to 3, 5.5—
18 * 2—4 cm, light brown, reaching or surpassing
ground level. Leaves solitary; petioles 1-2 m long
above ground, 3—4 cm diam. at midpoint, brownish
green, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern,
smooth or usually with spiny projections; juvenile
blade sagittate, or sagittately lobed; mature blades
spreading horizontally, 1—1.2 m diam., thinly cori-
aceous, sometimes fenestrate throughout the blade.
never variegated, dark
markings, glossy and dark green above, semiglossy

without raphide cells

and medium green below; middle division twice tri-
45-58 X 40-60 cm. with
terminal subdivision consisting of 3 sections, with

chotomously branched,

each basal subdivision consisting of many seg-
divisions twice dichotomously
branched, < X 40-55 ст,
division consisting of 2 sections, with basal sub-

ments; lateral

45-55 with terminal sub-
division consisting of many segments; terminal and
subterminal sections free, each consisting of a few
segments; leaf segments bilobed, broadly oblanceo-
ate, more than 5 cm wide on each side of the major

ribs, ovate or oblong, at least some of the basal
segments free from each other, often with contrast-
ingly smaller rounded or triangular segments alter-
nating with larger segments; apices acuminate, or
acute; ultimate segments 10—20 cm long, confluent
with penultimate segments; other segments 6.5-19
cm long; penultimate segments confluent with the
subterminal sections; medial segments free from
basal subdivisions; basal segments present, free
from each other; rachises patterned similar to pet-
iole but in much paler shades, smooth; tertiary
veins obscure above and conspicuous below; brac-
teoles 2 or 3, 4—20 X 2.5—4 cm, pink to dark brown,
the longest one much shorter than the peduncle,
partially covering the base of the peduncle. /nflo-
rescence solitary, appearing before new leaf; pedun-
cle 30-70 cm long above ground, 1-2 ст diam. at
midpoint, less than half as long as the petiole, mot-
tled similar to petiole but deeper in color, brownish
green, smooth; spathe (10—)13—20(—28) cm long,
(1-)2.5-3.5(—6) cm wide, cymbiform or non-cym-
biform, constricted at a certain point and differen-
tiated into a proximal tube and a distal lamina
(blade), cucullate or non-cucullate, erect or slightly

arching, apex acuminate; inner surface glossy, pur-
ple-red, 3A cm
high, shorter than spadix or as long as spadix; outer

with translucent area obvious,

surface maroon, matte; margins wrinkled and some-
times lobed on each side, broadly overlapping at
the base; veins conspicuous inside and raised out-
side, similar to the spathe in color: spadix hidden.
stipitate, cylindric, brown or brown-purple, 3—1.9
X 0.8—1.2 cm at anthesis, never with appendages
at apex: stipe 0.5-0.7 cm long. 0.4-0.6 em diam.
at anthesis. Flower tepals 4 to 6, 1-2.5 X 0.5-1
mm, light brown tinged green or brown-purple: sta-
mens 6 to 9; filaments 0.7-2.2 mm long; anthers
0.5 mm long, slightly exserted: ovary 3-locular, pale
green: stigma 3-lobed; style 1-2 mm long above
tepals, purple, persistent. /nfructescence with spadix
6-15 cm long, 2-2.5 em diam. in fruit: berries l-
0.5-0.7 ст thick.
apically truncate;

іо 3-seeded, 0.7—1 em diam.

subglobose, 4- to 5-angular,
young berries dark green; mature berries’ color un-
known, seeds
0.4-0.6 cm diam.,

raised; dorsal ridge 1,

drying with abundant reddish dots:

reniform, light brown, laterally
more

obvious, continuous,

than 1 mm thick, 0.5 mm high, smooth on both
sides.
Phenology. Flowering from June to August.

sometimes in February; mature fruits collected in
January and February.
Distribution and habitat. Dracontium plow-

manii is endemic to Peru, ranging from Junín
through Cuzco to the Tambopata area in Madre de
Dios. It occurs in Tropical moist forest (T-mf) and
е moist forest (P-mf) life zones (Holdrid-
). at elevations of 200 to 720 m.

Dracontium plowmanii is charac-

ge et al., 197

5
terized by the often undulate or lobed spathe mar-
gins and small seeds with a single continuous dor-
sal ridge. It is easily confused with D. spruceanum,
which differs in having larger seeds to 0.7 cm long.
with three dorsal ridges, and usually entire and
non-wavy spathe margins. It is also superficially
similar to D. longipes, which differs by having a
straight non-wavy margined spathe and seeds that
have three obvious dorsal ridges. This species is in
cultivation at the Missouri Botanical Garden, Marie
Selby Botanical Gardens, and the Dewey Fisk
Nursery in Florida.

This new species is named in honor of the late
Timothy Plowman, whose numerous collections of
Araceae include many live collections introduced
to horticulture as well as the type specimen of this

species.
Paratypes. PERU. Cuzco: Atavala, Vargas 13433
(US). Junín: San Luíz de Shuara, Plowman & Kennedy

648

Annals of the
Missouri Botanical Garden

5654 (К, GH). Loreto: Yarina at Río Tapiche, Vasquez et
al. 4841 (MO). Madre de Dios: Cocha Cashu, Parque
Manu, Nuñez 1885 (F); Manu, Par. Nac. del Manu on Río
Manu, Coc cha Cashu Station, Foster 9558 (F, MO); 12 km
Gentry & Núñez 69383 (МО);
) air km or 70-80 river km SSW of Puerto
ildonado, s 1520 (MO, MOL).
Cultivated plants. Peru. Lima, sent by Anderson, cult.
Fa airchild Tropical Garden, Miami, Florida, (same as Selby
2421), M. Madison £d (SEL); 17 0 vd ба col-
jec te by O. Phillips, 5 Sep. 1994, cult. а ‚ G. Zhu
12 2 (МО); from Selby Garde ns (76- 1 жн al MBG,
ы ‘hered as T Plowman 5654], Croat 73989 (MO), (
Zhu 1482, 1498 (MO); from Selby Gardens (77-2421),
cult. at MBG [vouchered as M. Madison 4229], G. Zhu
1446, 1447, 1480, 1487, 1496, 1496A (MO); from Selby
Gardens (76-575), cult. at MBG [vouchered as J. Plow-
man 5654), Christenson 1287, 1490, 1491 (MO), G. Zhu
1466 (MO)

=

e ire

=

18. Dracontium polyphyllum L., Sp. Pl. 967.
753, non Dracontium polyphyllum Houtt.,
Handl. Pl.-Kruidk. 11: 199, 1773-1783, hom.
illeg. [= Amorphophallus giganteus Blume |:
nec igi polyphyllum Vorst. f., Diss. Pl.
Esc. 61, n. 29. 1786, hom. illeg. [= Amorpho-
phallus 1 (Dennst.) Nicolson]; nec
Dracontium polyphyllum Dennst., Schluess.
Hort. Malab. 38. 1818, hom. Шер. |= Amor-
phophallus dubius Blume |: nec Dracontium po-
lyphyllum A. Cunn. ex A. DC., in DC., Prod.
16(2): 534. 1866, hom. Шер. | = Bowenia spec-
tabilis Hook. f. J. TYPE: plate 93 Herm.

Parad. Bat. 1698 (lectotype, designated by
Hay (1992: 189)); French Guiana. Saül, 13
Feb. 1993 (T. B. Croat 74210) |cultivated

plant at MBG], G. Zhu 1462 (epitype, desig-
nated by Zhu & Grayum (1995: 521), MO!)

Figures 1B, 1C, 21

=

Dracontium asperum К. Koch var. wallisii Engl. in Ma
*
l lid.

Fl. Bras. 3(2): 126. 1878. Syn. nov.

wallisii Regel, Gartenfl. 322. 1861, nom. invalie

TYPE: Brazil. Рага: Martius s.n. (holotype, not seen,

p xobably B or M).

Echidnium regelianum Engl., in DC., Monogr. Phan

286. 1989. Syn. nov. a шич, regelianum (E “1 )

Bogner, Aroideana 8: 78. 1985. Echidnium spru-

ceanum Regel, Gartenfl. 15: 98, 1. 503. 1 7 non
Schott. TYPE: tab. 503 in Gartenfl., 1866: 98 (le

буде; designated by Bogner (1985: 78)).
Tuber hemispherical or rounded, 6-10 cm diam..
5-8 em thick,

brown below, 5—15

flat above, rounded and white to

cm below ground level; tuber-

cles few, cylindrically elongated or irregular-

shaped, 0.5 em diam., 1 em long, borne around the
periphery of tuber; roots white, to 0.3 cm diam.:
cataph ylls З to 5, 3-16 ст long, 1-2 em wide. light
brown, reaching or surpassing ground level. Leaves
solitary or sometimes two or more per tuber: petioles

1-2 m long above ground, 2-3.5 em diam. at mid-
point, dark green or brown-green, contrastingly
mottled with dirty white or pale green blotches and
forming a reptilian pattern, usually smooth in upper
half and with irregular protuberances in lower half;
juvenile blade sagittate, or sagittately lobed; mature
blade spreading horizontally, 0.8-1 m diam., papy-
raceous, sometimes fenestrate, sometimes variegal-
ed, with abundant raphide cells (sometimes), glossy
and dark green above, semiglossy and medium
green below; middle division twice trichotomously
branched, 50-80 & 50-75 em, with terminal sub-
division consisting of three sections, with each bas-

al subdivision consisting of many segments; latera
divisions twice dichotomously branched, 50-80 X
45-70 cm, with terminal subdivision consisting of
with basal subdivision consisting of

апу segments; terminal and subterminal sections
confluent or free, each consisting of a few segments
or each consisting of many segments: leaf segments

2 sections,

bilobed or trilobed, oblanceolate, more

than 5 em wide on each side of the major ribs,
oblanceolate or elliptic, at least some of the basal

broadly

segments free from each other, often with contrast-
ingly smaller rounded or triangular segments alter-
nating with larger segments; apices caudate or acu-
minate; ultimate segments 12-20 cm long, free from
penultimate segments or rarely confluent with pen-
ultimate segments; other segments 5—15 cm long;
penultimate segments free from subterminal sec-
tions; medial segments free from basal subdivi-
sions, or rarely confluent with the basal subdivi-
sions; basal segments present, free from each other:
rachises patterned similar to petiole but in much
paler shades, with spiny projections (sometimes):
tertiary veins obscure above and weakly raised be-
low: 18 X 1.5-2 dark
brown to pink, the longest one + as long as the
peduncle or shorter than the peduncle, covering up
to 1/3 of the spathe. Inflorescence solitary or rarely
two, appearing before new leaf; peduncle 5-18 cm
long above ground, 0.5-0.8 em diam. at midpoint,
often almost completely subterranean (less than 10

bracteoles 3 or 4, cm,

cm above ground level), scarcely mottled, gray or
whitish green, with irregular very weak protuber-

ances; spathe 6-12 cm long, 3-5 em wide, cymbi-

form, cucullate, arching to 45°, apex acuminate; in-

ner surface semiglossy, violet-purple, with
translucent area obvious, 0.5-1 cm high, shorter
than spadix; outer surface maroon, tinged green,
sometimes wrinkled,

matte: entire or

scarcely to slightly overlapping at the base; veins

margins

obscure to conspicuous inside, conspicuously dark-
er or paler than the spathe, purple: spadix exposed,

stipitate, cylindric, narrower at apex, purple, 2.5—

Volume 91, Number 4 Zhu & Croat 649
2004 Revision of Dracontium

A

Figure 21. A-D, Dracontium Lyin Wise —A. nflorescence at anthesis in face view (G. Zhu 1462). B. In-
fructescence with pe rsistent spathe (Croat 74210). . Habit of plant with leaf and infructescence (Croat 74284). —
D. Seeds in side view (Croat 7 74211 ))

650

Annals of the
Missouri Botanical Garden

4.2 cm long, 1—1.2 em diam. at anthesis, never with
appendages at apex; stipe 0.5-0.8 cm long, 0.4-
).8 em diam. at anthesis, pale green or light brown.
Flower tepals 4 to 5(to 6), 2-4 mm long. 1-2 mm
wide, purple or light brown: stamens 5 or 6 to 7:
filaments 2-3 mm long; anthers 1-2 mm long.
slightly exserted; ovary 3-locular or 3- or 4-locular
(rarely), pale green; stigma 2-lobed or often 3-
lobed; style 0-2 mm long above tepals, purple, per-
sistent. Infructescence with spadix 5-16 cm long.
3—4 cm diam. in fruit; berries 3-seeded, 0.5—0.7 cm
diam., 1-1.5 em thick, subglobose, 3- to 6-angular,
apically subtruncate; young berries pale green; ma-
ture. berries greenish purple: 0.5-0.7 cm
diam., reniform, light brown, laterally raised: dorsal

seeds

ridges obvious, 1, continuous, with the central ridge
contrastingly raised, more than 1 mm thick, 0.5—
mm high, warty along both sides, appearing as
strongly reduced lateral ridges. Chromosome num-

ber 2n — 26 (Croat 74210).

—

Phenology. Flowering from December to June,
with the peak probably from December to January;
mature fruits are only collected in February.

Distribution and habitat, Dracontium polyphyl-
lum ranges from the Atlantic coast of Surinam and
French Guiana to northern Brazil (Pará State) and
Amazonian Venezuela (Bolívar and Portuguesa
States). It occurs in Tropical moist forest (T-mf) and
Premontane wet forest (P-wf) life zones (Holdridge
1971), at elevations of 0 to 220 m.
"Mai-eri" (Balée 2106, NY); “kao

et al.,

Local names.
aj" (Sauvain 175,

Discussion. Пеано polyphyllum is distin-
guished by its often subterranean peduncle, usually
broadly opened spathe with a glossy inner surface,
and smooth, laterally convex seeds. Historically, it
has been confused with D. asperum (see discussion
of D. asperum). It is also similar to D. guianense,
which differs in having the above-ground portion of
the peduncle much longer than the spathe. The
shape of the spathe of D. polyphyllum is similar to
that of D. dubium, but the inner surface of the
spathe is semiglossy in the former and is covered
with translucent scales in the latter.

Dracontium asperum К. Koch var. wallisii Engl.
is synonymized here under D. polyphyllum for the
first time. The name Dracontium asperum var. wal-
lisii had been synonymized with D. asperum pre-
viously (Engler, 1911). However, D. asperum var.
wallisii has a variegated blade, which shows that it
belongs to D. polyphyllum.

Under the name Echidnium spruceanum Schott,
Regel (1866: 98, t. 503) described a species based

on a plant collected by Appun, presumably in Ve-

nezuela, with a plate. This species was later named
as E. regelianum Engl. (1879: 286) in memory of
E. Regel, citing the plate of the plant published by
Regel (1866: t. 503). In the protologue of E. rege-
lianum, Engler (1879: 287) only mentioned the col-
and did not designate a
503) was designat-

lectors name “Appun”
type. The plate (Regel, 1866: t.
ed as a lectotype of E. regelianum by Bogner (1985:
78) when he made the combination Dracontium re-
gelianum (Engl.) Bogner. No herbarium material
related to the original description has been found.
All characters from the description and the lecto-
type suggest it is conspecific with D. polyphyllum.

Wallis (1861) collected a plant he called *Amor-
phophallus dubius (Dracontium polyphyllum)” on an
exploration trip to Pará in northern Brazil, and pub-
lished a sketch of the plant in its natural habitat
along with his field notes. Regel (footnote in Wallis,
1861: 332) suggested that the plant might be a new
species and later published a color illustration of
the same plant received from Wallis under the
name A. wallisii, with a clear statement that the
name was provisional and that it might end up be-
ing a "form" of an already described species (Re-
gel, 1862). Thus, according to Article 34 of the
current /nternational Code of Botanical Nomencla-
ture (Greuter et al., 2000), the name А. wallisii Re-
gel is of no taxonomic value. Engler (1878) intend-
ed to use the name A. wallisii as the basionym of
a new combination, D. asperum var. wallisii, but
this name is no longer considered published, so
actually Engler published a new name for his va-
riety. Engler provided a description and cited one
specimen he saw for this variety. Because Regel's
name is not validly published, this specimen must
be considered the type.

Additional specimens examined. BRAZIL. poa Lag-
eira, airstrip on Rio Maicuru, Strudwick et al. 3987 (MG,
NY); Altamira, Igarapé Ipixuna, affluent of Rio с. Ar-
aweté Indian Reserve, Balée 2106 (M( +
Itupanema, Sao C an km 12, Gély 60 (MG); Conceigáo
do Araguaia, ca. 20 km W of Redengáo, near dp iy
Joáo & Trone amento Santa Teresa, Plow et al. 8
(МС, M Y); Oriximiná, Campos до Ari ылы а, ES я
че з P km N of Ponte do Rio Cuminá-Mirin

513 (MG). FRENCH GUIANA. Locality unkn
prieur s.n. (P), Richard s.n. (P), 5 407 (GH, NY,
US); Chemin de la source de Baduel, Pr pe 2191,
н (CAY); Colline du Montabo, Riera 415 (CAY); Mon-

tagne des Nouragues, B: de Г Арр rouague, Arataye,
i ocu, Bassin dt

е
S of Cayenne, 105 Route de Montagne
"Trésor, ona: side trail to Placer Trésor, Feuillet 3993

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

(CAY, К, , P, U, US); 1 эуе ы Чи Маһигу, rs du
Rorota, ‘wn 38043 (NY, P); Piste Sophie, La Gréve
Hallé 7 AY, Р, ; Route 2 Rorota, Paris 36
(CAY); i. Sulack posce 19 CAY): Saül N of
han Claires along rd. to Béllizon, vns 74210 (CAY,
K. US): Saül, Saint Laurent du Maroni, Moretti 122

Ж m Saut м bassin de
M.

12734 (CAY). SURINA ч creek
area, Bosbeheer 0845 (U): Sectie O, Pulle 161 (U). Bro-

kopondo: Banafokonde on Surinam Es серн 175
(BBS, CAY W
16153 (BBS).
bied. Sang 16866 (BBS): pane hice, Hur 9845
(BBS). 5 Rijsdijkeg. ca. 25 km 1 s
0 0 4608 (U); achter Cultuurtuin, Stahel s.n
VENEZUELA. a : Río Caura, Caño La Ceiba UA
Cumaca), А & Delgada 12940 (MO, 1 Por-
ol. Pozo Blanco, Mori et dl. Mn Y)
French Guiana. Cult. Paris d
‚ Mélinon s.n. (P); collected by Joep Moonen
received from J. Boos, cult. MBG. G. Zhu
Cayenne, cult. |
Croat 74210), G. Zhu 1462, 1513 (MO).
Santo, cult. MBG [vouchered as Croat 71785]. Zhu 1483,
1488 (MO): originally collected by Н. van der Werff, cult.
MBG [vouchered as Croat п Э Singapore. Ве-
hind repair shed, Nicolson 1119 (

inege-

uc l 993

19. wp ear prancei G. Zhu & Croat, sp.
А ҮРЕ: Brazil. Pico Rondon,
: нее Norte Hwy., 1?32'N,
mop W. 2 Feb. 1984, G. Prance, J. L. do
Amaral. J. Pipoly, A. Tavares, C. D. A. la Mota
& A. Cress 28732 (holotype, NY!). Figure 22.

nov. Amazonas:

N

Petiolus 1.6-2.5 m longus: pedunculus iig ‘rraneanus,
l-5 em longus: spatha (10)15-18 em lon 2—4 em
intus. velutina, purpurea: spadix

-1.2 em diam.; yaccae
semina brunneola vel fusca,

NE
>
85

tepala 5:
em diam.
0.5-0.6 em diam.

globosae, 1—1.2

Tuber hemispherical, 8-14 cm diam.. 6-9 em

thick. flat above. rounded and white to brown be-

low. 10-15 cm below ground level: tubercles abun-
dant, rounded, 0.5-1 ст diam., borne around the

periphery of tuber; roots whitish, to 0.3 mm diam.:
1-20 cm long.
pink to light brown, 5-15 em long above ground.

cataphylls 4 or 5. 2.5—4 cm wide,
Leaves solitary or sometimes two or more per tuber:
petioles 1.6-2.5 m long above ground. 2.5-3.5 em
diam. at midpoint, dark green, contrastingly mol-
tled with dirty white or pale green blotches and
forming a reptilian pattern, usually smooth in upper
half and with irregular protuberances in lower half:
juvenile blade sagittate, or sagittately lobed; mature
blade spreading horizontally, 1-1.2 m diam.. papy-
raceous, sometimes fenestrate. never variegated,
without raphide cells or dark markings. glossy and
medium medium
green below: middle division twice trichotomously

branched, 55-65 X 50-60 em. with terminal sub-

green above, semiglossy and

division consisting of 3 sections, with each basal
subdivision consisting of many segments: lateral di-
visions once or twice dichotomously branched, 50—
60 55—00 cm,

sisting of 2 sections, with basal subdivision con-

with terminal subdivision con-

sisting of many segments; terminal and subterminal
sections free from each other, each consisting of
many segments; leaf segments often entire, broadly
oblanceolate, more than 5 em wide on each side of
the major ribs, oblanceolate, mostly free from each
other in each division, without contrastingly smaller
rounded or triangular segments; apices acuminate:
ultimate segments 10-13 cm long. free from pen-
ultimate segments: other segments 3-12 em long:
penultimate segments free from the subterminal
sections; medial segments free from basal subdi-
visions: basal segments present, free from each oth-
er; rachises patterned distinct from petiole, pale
green, smooth; tertiary veins conspicuous above

7-14

em long. 3-5 em wide, pink and light brown, the

and weakly raised below: bracteoles 3 ог
longest one longer than the peduncle, slightly cov-
ering the base of the spathe. Inflorescence solitary
or sometimes two, appearing before new leaf; pe-
duncle 1-5 em long above ground. 1-1.2 em diam.
at midpoint, often almost completely subterranean,
scarcely mottled, brownish green or whitish tinged
3.2-4

em wide, cymbiform, cucullate, arching up to 45°,

pink, smooth: spathe (1015-18 em long.
apex acuminate: inner surface semiglossy or vel-
vety, maroon or blackish purple. with translucent
area obvious, 0.5-1 em high, shorter than spadix;
outer surface maroon (sometimes tinged green).
matte; margins entire, broadly overlapping in the
lower two-thirds: veins obscure inside and raised
outside, than the
spathe; spadix hidden, stipitate, cylindric, narrower

conspicuously darker or paler
at apex, purple or brownish purple. (2.5—)4—5 х
0.9-1.2 cm at anthesis, never with appendages at
apex: stipe 0.5-0.8 cm long, 0.5-0.7 em diam. at
anthesis, purple. Flower tepals 5. 1.5-2.5 mm long.
1-2 mm wide, purple or brownish purple: stamens
6 or 7: filaments 1-2.5 mm long: anthers 0.5 mm
long. completely exserted; ovary 3-locular, pale
green; stigma 3-lobed: style 1-2 mm long above
tepals, purple, persistent. /nfructescence with spadix
5.5 em long. 2.4 em diam. in fruit; berries 1-seeded,
1-1.2 cm diam., 0.8-1 em thick. subglobose, 3- to
6-angular, apically truncate; young berries light
green; mature berries color unknown, with abun-
dant raphide cells: seeds 0.5—0.6 cm diam., reni-
form, light brown or dark brown, laterally flattened;
sparsely beset with irregular warts dorsally. dorsal
ridges obscure. Chromosome number 25 = 26

(Croat 73867).

652

Annals of the
Missouri Botanical Garden

ч y 7 С
ht.
* wt.

Figure

cut away to expose spadix.

DO

—D, 5 5 —A.
pical portion of le af blade (G. Zhu 1455). . Close-up of stigma (G. Zhu 1

MISSOURI

BOTANICAL GARDEN
HERBARIUM

N?

flor

4319849

scence in side view (C id (i oe —RB. Inflorescence with oo
5

Volume 91, Number 4 Zhu & Croat 653
2004 Revision of Dracontium
Phenology. Flowering known only in February: thick, flat above, rounded and white to brown be-

mature fruits are known only in May.

Distribution and habitat. — Dracontium prancei is
known only from Brazil in the states of Amazonas
and Roraima. It occurs in the Tropical moist forest
(Emf) life zone (Holdridge et al.. 1971). at eleva-
tions of 50 to 150 m.

Discussion. Dracontium. prancet may be con-
fused with D. asperum because of the similar sizes
and shapes of the spathe, but the latter species dif-
fers in having bracteoles much shorter than the pe-
duncles and never reaching the spathe (in contrast
to elongate bracteoles that subtend the entire pe-
duncle. even over the base of the spathe in D. pran-
cel). Dracontium prancei has a short peduncle up
to 5 em above ground while D. asperum has a pe-
duncle 5 to 17 em above ground. Live plants of this
species of unknown origin were widely distributed
by the Munich Botanical Garden under the name
D. polyphyllum, which differs from D. prancei in
having a much shorter spathe 6-12 cm long versus
(10—)15—18 cm long in D. prancel. The spadix is
usually exposed in D. polyphyllum and completely
embraced by the spathe in D. prancei. Dracontium
ргапсе is another species that is easily grown and
has great horticultural value. It grows rapidly, prop-
agales easily by tubercles, and blooms regularly in
cultivation. A plant of D. prancei is cultivated
the Climatron® at the Missouri Botanical Garden.

Dracontium prancei is named in honor of Ghil-
lean Prance, whose many collections throughout the
Amazon basin of Brazil include the type specimen
of this species.

Paratype. BRAZIL. Roraima: SEMA Ecol. Res.. S
of Cachoeira de E 24 July 1987, Milliken et al.

511 (K).
Cultivated plants. Origin unknown.

rio ted by J.
Garden. Germany. 28
z. Zhu 1501 (MO). Oe
inally feti Munich Botanic al us n.

from W. Hetterscheid in Holl: and, cult.
/3867 (MO), G. Zhu 1458, 1463 (MO).

recelv ed

B. Croat

Ge ша
MBG, 7.

20. Dracontium purdieanum (Schott) Engl..
Pflanzenr. IV. 23C (Heft 48): 45. 1911. Ophi-
one purdieana Schott, Oesterr. Bot. Wochenbl.
7: 101. 1857 PE: Colombia. Magdalena:
Santa Marta, 1845, W. Purdie s.n. (holotype.
K!). Figure 23.

Dracontium aricuaisanum G. S. Bunting, Tops 60:

1-302. 1 . Pe

985. TYPE: tod. Zulia:

30 2:
ijá, outskirts of Est. Hidrol. Aricuaisá-Pie de Ma
k anlai $ 3355, 100-250 m. 25 Feb.-3

Mar . Bunting, б. e ra & ü Lobo
12555 pe, NY isotype. VEN!)

Tuber hemispherical, 4-6 cm diam., 3.5—4 cm

low. 9-16 em below ground level: tubercles abun-

dant, obovoid, 0.5-0.9 em diam., 1—1.5 cm long.

borne around the periphery of tuber: roots white,

З mm diam.; cataphylls З to 4, (3-)9-17 cm long.

2-3 cm wide. whitish to light brown, reaching or
surpassing ground level. Leaves solitary; petioles 1—
1.8 m above ground, 2.5—4 cm diam. at midpoint,
dark green or brownish green (tinged gray). con-
trastingly mottled with dirty white or pale green
blotches and forming a reptilian pattern, smooth:
juvenile blade sagittate, or sagittately lobed: mature
blade spreading horizontally, 0.8—1.2 m diam., pap-
yraceous, sometimes fenestrate, sometimes varie-
gated, with abundant raphide cells and dark mark-
ings (1-2 mm long), semiglossy and medium green
above, glossy and dark green below: middle division
90-65 X 40-55
cm. with terminal subdivision consisting of 3 sec-

twice trichotomously branched,

tions, with each basal. subdivision consisting of
many segments; lateral divisions twice dichoto-

50-60 х 45-50 cm. with ter-
minal subdivision consisting of 2 sections,

mously branched,
with
basal subdivision consisting of many segments: ter-
minal and subterminal sections free, each usually
consisting of a single segment; broadly oblanceo-
late. more than 5 em wide on each side of the major

ribs. oblanceolate, mostly free from each other in
each division, without contrastingly smaller round-

ed or

=

triangular segments; apices acuminate. «
acute, or caudate (sometimes); ultimate segments 9—
20 cm long. free from penultimate segments: other
segments 1.5-10 cm long: penultimate segments
free from. subterminal sections; medial segments
free from basal subdivisions; basal segments pres-

free from each other: rachises patterned dis-
tinct from petiole, pale green, smooth; tertiary veins
obscure above and weakly raised below; bracteoles
З to 4, 9-25 em long, 2-3 cm wide.

the longest one + as long as the peduncle. reaching
8 8 | B

light brown.
the spathe. Inflorescence solitary, appearing before
new leaf: peduncle 0—5 em long above ground, 0.8—
| em diam. at midpoint, often almost completely
subterranean (0—5 em above ground level), scarcely
mottled, brownish green, with irregular. protuber-
ances or spiny projections (sometimes); spathe 6—
15 X 1.8-3.5 cm,
certain point and differentiated into a proximal tube

non-cymbiform, broadened at a
and a distal lamina (blade), non-cucullate. arching
1.5-3 X 1.8-3.5
widest point: lamina 2 to 3 times longer than the

to 45°, apex acuminate: cm at
tube; inner surface covered with dense, translucent
scales 1-2 mm long, violet-purple or olive-brown.
with translucent area obscure: outer surface violet-
purple, tinged green, matte; margins entire. broadly

654

Annals of the
Missouri Botanical Garden

0.6 cm

amet
Figure 23. A-D, Drac ontium purdieanum. A, B, (Aristeguteta s. n —A. Inflorescence at anthesis. Photo by J
Bogner. —B. Cultivated plant with leaf at Munic h Botanic ‘al Garden. —C. Type specimen of D. aricuaisanum G. S

Bunting. —D. Seeds in late 5 view (Bunting 1146.

Volume 91, Number 4
2004

Zhu & Croat 655

Revision of Dracontium

overlapping at the base; veins conspicuous inside,
conspicuously darker or paler than the spathe, pur-
ple: spadix exposed, sessile or stipitate, cylindric,
brownish purple, 2—4 em long, 0.5-1 em diam. at
anthesis, often with one to a few appendages at
apex, 0.2-0.5 cm long when present; stipe 0.8 cm
long. 0.5 em diam. at anthesis, light brown. Flower
tepals 4 to 6(to 7), 1-2 mm long, 1 mm wide, green
or light brown; stamens 6 or 7; filaments 1-2 mm
long: anthers 0.5 mm long, slightly exserted; ovary
3- to 5-locular, pale green; stigma 3- or 4-lobed:
style 0.5-1

persistent. Infructescence with spadix 4.5-5 ст
long, 3.5—4 em diam. in fruit; berries (08. to 4(5)-
1-1.3 em thick, subglo-

mm long above tepals, peu not

seeded, 1-1.2 ст diam.,
bose, 3- to 6-angular, apically truncate; young ber-
ries dark green: mature berries purplish red,
sometimes with abundant raphide cells: seeds 0.5—
0.7 em diam., reniform, dark brown, laterally de-
pressed: dorsal ridges obvious, 3 continuous ridges
(sometimes with 1-2 strongly intermediate inter-
rupted dorsal ridges), less than 0.5 mm thick, 0.3
mm high, warty along ridges. Chromosome number
1989).

2n = 26 (Aristeguieta s. H.; Petersen,

Phenology. Flowering from February to March:
mature fruits from April to May.

Distribution and habitat. Dracontium purdiean-
um is known only from the Caribbean coastal de-
partments of Atlántico, Magdalena, and Bolívar in
Colombia, and Zulia. Venezuela. It occurs in Trop-
ical moist forest (T-mf) and Premontane moist forest
1971) along the

coast, at elevations from sea level to 250 m.

(P-mf) life zones (Holdridge et al.,

Discussion. | Dracontium purdieanum is charac-
terized by having the inner surface of the spathe
densely covered with translucent scales (1-2 mm
long). and a spadix that often has appendages at
the apex. This species is vegetatively similar to D.
dubium but differs from that species in having
seeds with 3 continuous ridges (sometimes with 1—
2 strongly intermediate interrupted dorsal ridges).

In 1845, a year after Schomburgk's expedition to
British Guiana (Guyana), William Purdie collected
a second plant presently included in Dracontium
from the vicinity of Santa Marta, Magdalena De-
partment, Colombia. This collection was named
Ophione purdieana Schott as a new unispecific ge-
nus, which differs from Dracontium in having a
long-acuminate spathe (Schott, 1857a). Later, En-
gler (1911) placed this species in Dracontium, cit-
ing “D. purdieanum (Schott) Hook. f. in Bot. Mag.
(1973 However,
no such combination was made by J. D. Hooker in
himself. validly

in observatione ad tabulam 6048."

—

that publication. Instead, Engler

м

published the combination (1911: 45), citing the
basionym after D. purdieanum, which combination
must therefore be attributed to Schott) Engler”
according to the Code (Art. 46, Greuter et al.,
2000)

In the protologue of Ophione purdieana Schott
(1857a: 101), there is no explicit type designation,
but it was clearly stated that the name, which hon-
ors the collector, was based on a gathering made
from "St. Marta.”
mention of a single gathering as indication of the
type (Art. 37.3, Greuter et al., 2000). A specimen
(Purdie s.n., К, 1845) collected near Santa Marta
in Colombia is evidently the same one used by
Schott when describing 0. Schott
(1858b: t. 89) published an illustration of the spe-
cles a year after its original description. The spathe

by “Purdie” This constitutes

purdieana.

in the illustration matches that of Purdie s.n. in
great detail. Purdie s.n. can therefore be regarded
as the holotype of O. purdieana Schott.

More than a century after its discovery. Dracon-
tium purdieanum was re-collected and redescribed
by Bunting (1986) as D. aricuaisanum from Ari-
ie de Monte in Zulia State,
Bunting's new species differed from D. purdieanum

cuaisá—Pie Venezuela.

in no significant way.

COLOMBIA. Atlán-

Candelaria,

Additional specimens examined.
tico: along trail rom Luruaco to Pinar de
5 1161 (F). Bolivar: lands of Loba, Caño Papayal,
Strella, Сыт 349 (GH, US). VENEZUELA. Zu-

Aricuaisá [Ariguaisá| & Pie de Monte on Rio
SW of Machiques by air, Liesner & Gon-

Nin uela. Zulia, Aricuaisá, cult. at
Germany, M).

Cultivated plants.
Munich Botanical Garden, €

je

Aristeguieta s.n.

21. Dracontium soconuscum M; а А тег.
Midl. Naturalist 41: 494. 1949. TYPE: Mexi-
co. Chiapas: Soconusco, Santa ү 16 km
W of Acapetagua, 30 m, Jan. 1947. E. Matuda
17780 (lectotype, MEXU
85137! pro parte, inflorescence; isotypes,

MEXU!, №Ү!). Figure 24.

designated here.

— P Croat, Selbyana 1: 168. 1975. Syn.

PE: Panama. Canal Zone: Barro Colorado Is-

an near end of Zetek trail, 30 June 1972, R. Dress-
ler s.n. (holotype, MO!).

Tuber hemispherical or rounded, 4-7 cm diam.
5-9 cm thick, flat above, rounded and white to
brown below, 4—45 em below ground level; tuber-
cles few, cylindrically elongated, 0.5-0.8 cm diam.,
0.5-1 cm long, borne around the periphery of tu-
ber; roots whitish or sometimes tinged green, to 3
mm diam.; cataphylls З or 4, 3-47 cm long, 2-3.5
cm wide, pink or light brown (when dried), reaching

656

Annals of the
Missouri Botanical Garden

Figure 24. A-D, 5 soconuscum.
Photo by Bogner. B, C, ¿hu
ateral view (Bartlett & Pat unes

—A.

. Inflorescence side

Cultivated bs

1.
ie м

iar T.
=L;

0.8 cm
A

Inflorescence

al

anthesis in face view.

saf blade adaxial surface. —D. See

s in

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

657

or surpassing ground level. Leaves solitary or some-
times two or more per tuber; petioles 1—1.8 m long
above ground, 3—5 cm diam. at midpoint, dark
green or gray or whitish green, sometimes tinged
mottled,

smooth in upper half and with irregular protuber-

brown or red-brown, weakly usually
ances in lower half; juvenile blade sagittate, or sag-
to the
petiole spreading horizontally, 1—1.2 m diam., sub-

ittately lobed: mature blade ascending to 45°

coriaceous papyraceous, sometimes fenestrale, nev-
er variegated, without raphide cells or dark mark-
ings, semiglossy and dark green above, matte and
medium green below; middle division 3 times or
0.8-1.5 0.6-1
em, with terminal subdivision consisting of 3 sec-
f
many segments; lateral divisions 3 times or more
dichotomously branched, 0.8-1 х 0.5-0.8 em, with
terminal subdivision consisting of 2 sections, with

more trichotomously branched,

lions, with each basal subdivision consisting «<

basal subdivision consisting of many segments; ter-
minal and subterminal sections free. each consist-
ing of segments; leaf bilobed,

many segments

broadly oblanceolate, more than 5 em wide on each
side of the major ribs, oblanceolate or orbicular-
ovate, at least some of the basal segments free from
each other, often with contrastingly smaller rounded
or triangular segments alternating with larger seg-

ments; apices acuminate, or ultimate

7-17

ments or

acule; seg-

ments em long. free from penultimate seg-

rarely confluent with penultimate
segments; other segments 5-15 cm long; penulti-
mate segments free from subterminal sections; me-
dial segments free from basal subdivisions: basal
segments absent, free from each other; rachises pat-
terned similar to petiole but in much paler shades,
similar to petiole but in a much paler scale; tertiary
veins obscure above and weakly raised below; brac-
teoles | to 3, 5—45 cm long. 1.5-2.5 em wide, pink
to light brown, the longest one longer than the pe-
duncle, covering the basal half or more of the
spathe. /nflorescence solitary or rarely two, appear-
ing before new leaf; peduncle 4-45 ст long above
ground, 0.8-1.2
completely subterranean (0-5 em above ground
level), scarcely mottled, whitish tinged pink,
smooth; spathe 6-8(10) em long, 3—4

non-cymbiform, constricted at a certain point and

cm diam. at midpoint, often almost

„Жм,

6) cm wide,

differentiated into a proximal tube and a distal lam-
ina (blade), cucullate, arching 45°-90°, apex acu-
minate; 1-3 em long. 2.5—4(5) em wide at widest
point; lamina similar to the tube in length (or slight-
ly longer): inner surface glossy, violet-purple or ma-
гооп, with translucent area obscure; outer surface
olive-brown or maroon, semiglossy; margins entire,
broadly overlapping in the lower half; veins obscure

inside or raised outside, similar to the spathe ii

color, purple; spadix а brin slipitate, Ee
violet-purple, 1—4 X 0.5-1 ст at anthesis, often
with several appendages at apex, 0.5-0.8 ст long
when present; stipe 0.3-0.7 X 0.5-0.6 em at an-
thesis, light brown. Flower tepals (4)5 or 6(8), 2—
6
7(9); filaments 1—1.5 mm long; anthers 1-2 mm

2.5 mm long, 1 mm wide, dark purple: stamens (5

=o

ae slightly exserted; ovary 2- to 5-locular, pale
green; stigma 3-lobed; style 0-1 mm long above
tepals, dark purple, not persistent. Infructescence
with spadix 4-10 cm long, 2-3.5 ст diam. in fruit:

berries 4-seeded, 0.8-1.4 cm diam., 1-1.5 em
thick, subglobose, 4- to 5-angular, apically trun-

cate; young berries dark green; mature berries pur-
plish brown, with abundant reddish dots: seeds 0.6—
0.9 em long, 0.5—0.6 em diam. (wide), reniform or
triangular (+), dark brown, laterally depressed:
dorsal ridges obvious, 3, continuous, monomorphic,
more than 1 mm thick, 0.1-0.5 mm high, warty
along both sides, appearing as strongly reduced lat-
eral ridges.

Phenology. Flowering from October to April:
mature fruits from April to August.

Distribution and habitat. The northernmost
species of the genus, Dracontium soconuscum is
known from the Pacific slope in southern Mexico
(Chiapas) and northern Costa Rica (Guanacaste.
Alajuela, Puntarenas), and on the Caribbean slope
in central Panama (Canal Zone). It occurs in costal
lowland thicket or bushes of the Tropical moist for-
est (T-mf) life zone (Holdridge et al., 1971), from
sea level to about 1100 m.

Local names. “Cola de tigre" (E. Matuda
17780, MEXU, NY).

Discussion. Dracontium. soconuscum is easily
confused vegetatively with D. grayumianum, but
that species differs in having seeds with five or six
strongly interrupted dorsal ridges, whereas D. so-
conuscum has seeds with three obvious and contin-
uous dorsal ridges.

According to the protologue, the type of Dracon-
E. Matuda 17780, consists of a
holotype in the Matuda Herbarium (CHIS) and two
isotypes (MEXU 6739, F). The holotype was later
transferred to MEXU (MEXU 85137) and the iso-

type intended for F was evidently sent to NY in-

tium. soconuscum,

stead. The type is a mixed collection of two gath-
erings prepared by the same collector in January
and May, 1947, respectively. Since a type can only
be a single gathering (Art. 8, Greuter et al., 2000),
the inflorescence on MEXU 85137 is designated
here as the lectotype of D. soconuscum.

There are three other gatherings existing under

658 Annals of the
Missouri Botanical Garden
the same collection number: Matuda 17780 thick, flat or slightly convex above, rounded and

MEXU 47893) collected from Cruz do Piedra, Jan-
uary and May 1947; Matuda 17780 (MEXU 85107)
collected from Nandolopez, January and May 1947
and Matuda 17780 (MEXU 141842) collected жи

Santa Teresa, Acapetagua, on 14 July 1947.

„—

Additional specimens examined. COSTA RICA. Ala-
juela: Finca Carlos Gómez, Orotina, Chacón 1414 (MO);
La Balsa de Río Grande, Pittier 3650 (US), Guanacaste:
Rio Higuerón, near Taboga, Liesner et al. 2720 (MO)
Puntarenas: rd. to Monteverde, Luteyn 3394 (DUKE);
Garabito Canton, a Biol. rd along S side of Rio
Grande de Tárco from Carretera Constanera to Rio
Carara, Grayum et e 11108 (MO) "MEXIC O. Chiapas:
Mazapa, 10 km E of Motozintla, Garcia et al. 1527 (BM).

A. Canal Zone: Pittier 3429 (US); Barro Colo-
rado Island, Zetek Trail, Croat 27795 (MO); Juan Mina,

Chagres River, Bartlett & Lasser 16831 (F, MO, NY); vic.
Summit Hills G Croat. 27794 (MO). Coclé:
3427 (MO). € Colén: Achiote, 1974,
PMA); Gamboa Country Club Mari-
F). Panamá: Río Agua Clara, lcantí,

—

— 5

na, Garwood 1639А
Gentry 2598 мо).

Cultivated plan Panama. Barro Colorado
cult. башы Garden [vouchered as Croat
Colón, Achiote, STRI [vouc в red
a. 1502 (MO); Canal Area, n.
Fairchild 2 ‘al Garden, Miami, Florida, U.S.A.,
4115, 4249 (FTG); cult. Selby Gardens, Madison babe
(SEL); cult. by Dewey Fisk, Florida (received from
Boos), G. Zhu 1485 (MO).

Island,

22. Dracontium келке (Schott) G. Zhu,
Novon 6: 308. 1996. Echidnium spruceanum
Schott, Oesterr. $e РА 8: 350. 1858. Cyrtos-
perma spruceanum (Schott) Engl., Martius, Fl.
Bras. 3(2): 118. 1878. TYPE: Brazil. Amazon-
as: Sáo Gabriel, May 1852, K. Spruce 2406
(holotype, K!). Figures 3C, 3D, 25, 26.

еа Hook. f., Bot. in ч 6523, 1880. Syn.
TYPE: Colombia. Apr. . E. Brown s.n.
(holotype, K! [3]). [Cultivated a by Mr. Bull. orig-
inally collected by Carder in Colombia, locality un-
known.]
Dracontium Engl., oe 4, Fam.
23C(44). 1911. Syn. nov. TYPE: Costa Rica. Limón:
Talamanca, forest of Shirones, 100 n m, Feb. 1895, H.

costaricense

Pittier 9232 (holotype, BR!; isotype, B!).
Dracontium trianae E. ngl.. Pflanzenr. 4, Fam. 23C(44).
911. Syn ‚ TYPE: Colombia. Meta: Villavicen-

cio, 400 m, p 1856, J. J. Triana 691 een ee
designated by Zhu (1996: 309), BM!; isotype, COL

).
ö loretense K. Krause, Notizbl. Bot. Gart. Ber-
lin-Dahlem 11: 617. 1932. Syn. nov. TYPE: Peru.

ie " lower Río Huallaga, 155-210 m, Oct.- Nov.
929, L. Williams 5144 (holotype, Fl; isotype, US!).

—

О? үт m K. Krause, Notizbl. Bot. Gart. Ber-
lin-Dah lem Pe : 940. Syn. nov. TY PE: Ecuador.
io 1100 m, 16 Nov. 1938, A.

Schultze- dogs d 2998 ias
Schultze-Rhonhof 303

B! [on sheet with

Tuber hemispherical, 4-18 cm diam., 3-10 cm

white to brown below, 15-40 em below ground lev-

rounded, 0.5-2 em diam.,

el; tubercles abundant,
borne around the periphery of tuber; roots to 4 mm
diam.; cataphylls to 3, 10—40 cm long, 2—4 ст
wide, pink to light brown, reaching or surpassing
ground level. Leaves solitary; petioles 1-3 m long
above ground, 1.24 em diam. at midpoint, dark
green, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern, usu-
ally smooth in upper half and with irregular pro-
tuberances in lower half; juvenile blade sagittate,
r sagittately lobed; mature blade spreading hori-
subcoriaceous to thinly

€
zontally, 0.9-1.5 m diam.,
rarely fenestrate, never

-

coriaceous, variegated,
without raphide cells or dark markings (often), se-
miglossy and dark green above, matte and medium
green below; middle division once or twice trichot-
omously branched, 47-60 X 45-55 cm, with ter-
minal subdivision never divided into sections, with
each basal subdivision consisting of many seg-
lateral divisions twice dichotomously
branched, 45-62 X 50-60 em, with terminal sub-
division consisting of 2 sections, with basal sub-

ments;

division consisting of many segments; terminal and
subterminal sections often free, each consisting of
many segments; broadly oblanceolate, more than 5
em wide on each side of the major ribs, oblanceo-
late or elliptic, mostly free from each other in each
division, without contrastingly smaller rounded or
triangular segments (often); apices caudate; ulti-
male segments 12-35 cm long, confluent with pen-
ultimate segments or free from penultimate seg-
ments; other segments 4.5-30 cm long; penultimate
segments free from subterminal sections; medial
segments free from basal subdivisions; basal seg-
ments present, free from each other; rachises pat-
terned similar to petiole but in much paler shades,
smooth; tertiary veins obscure above and weakly
raised below; bracteoles 1 to 3, 4—45 cm long, 1-3
cm wide, pinkish or light brown, the longest one
much shorter than the peduncle, confined at the
base. Inflorescence solitary, appearing before or af-
ter new leaf; peduncle 60-150 cm long above
ground, 2—3.5 cm diam. at midpoint, more than half
as long as the petiole or sometimes as long as or
longer than the petiole, mottled similar to petiole
but deeper in color, dark green or brownish н
smooth or with irregular protuberances in lower
half; spathe (20—)25-35 cm long, 3-6 cm wide,
non-cymbiform, constricted at a certain point and
differentiated into a proximal tube and a distal lam-
(blade)

erect or slightly arching, apex acuminate; 5-10 cm

ina or eymbiform (rarely), non-cucullate,

long. 3-6 em wide at widest point: lamina 3 to 5

Volume 91, Number 4 Zhu & Croat 659
2004 Revision of Dracontium

Figure 25. A-D, Dracontium spruceanum. —A. Habit showing flowering D (G. Zhu 1503). —B. Spathe a
anthesis split open to show the pale basal portion and the apadi f Zhu 1486). —C. Cultivated by Luis Bueno,
Miami. Petioles and juvenile infloresence. —D. Seeds in lateral view (Cerón 72368 ;

660 Annals of the
Missouri Botanical Garden

Figure 26. A, В. Dracontium spruceanum (G. Zhu 1486). —A. Side view of pistil showing unopened anthers. —
B. Apex of flower a tip of pistil with emerging threads of pollen.

Volume 91, Number 4
2004

Zhu & Croat
Revision of Dracontium

times longer than the tube; inner surface semiglos-
sy, maroon or olive-brown, with translucent area ob-
vious, 4-8 cm high, 1.5 to 3 times longer than spa-
dix: outer surface maroon, tinged green, or green,
matte; margins entire, broadly overlapping at the
base; veins obscure inside or raised outside, similar
to the spathe in color: spadix hidden, stipitate, cy-
lindric, purple or brownish purple or brown, (2.5—
)3—4(-0.5) X
pendages at apex: stipe 0.5-0.8 X 0.4-0.6 em at
anthesis, pale green or light brown. Flower tepals

0.6-1 cm at anthesis, never with ap-

A to 5, 1.5-2 mm long, 1-2 mm wide, purple: sta-

mens 6 to 11; filaments 1-1.5 mm long; anthers 0.5
mm long. slightly exserted; ovary 3-locular, pale

green; stigma unlobed, or 2- to 3-lobed; style 0.5—

mm long above tepals, purple. persistent. /nfruc-
tescence with spadix 8-16
berries 1- or 2-seeded, 0.5-0.7 ст diam.,

2.5—3.5 cm in fruit:
0.7—] cm
thick, globose or obliquely obovoid, apically round-
ed (sometimes slightly concave around the persis-
tent style); young berries medium green; mature
berries orange, without reddish dots and raphide
seeds 0.5). 7
elongated or rounded, reddish brown, laterally de—

cells; em long, 0.4-0.5 em diam.,
pressed; dorsal ridges obvious, more than 3, strong-
ly interrupted (often), with the central ridge con-
mm thick, 0.1—0.3

trastingly raised, more than

mm high, warty along ridges.

Phenology. Flowering throughout the year: ma-
ture fruits throughout the year.

Distribution and habitat. Dracontium sprucean-
um ranges from the Caribbean coastal plain of Cos-
ta Rica (Limón) to Colombia and Ecuador (on both
sides of the Andes) and Amazonian Ecuador, Peru.
Venezuela, and Brazil. It has also been collected
from Surinam. It occurs in Tropical moist forest (T-
mf). Premontane wet forest (P-wf), and Tropical wet
forest (V-wf) life zones (Holdridge et al., 1971), at
elevations of 25 to 1215 m.

Local names. “Tama kida bari” (La Rotta 586,
COL); “chupadera” (Archer 1729, US); °
(Idrobo & Cuatrecasas 2685, COL);
mandi” (Alarcon 62, QCA); “jergón sacha” (Vásquez
& Jaramillo 4938, MO).

Dracontium spruceanum is the most

“papayuéla”
“machaqui

Discussion.
morphologically plastic and widely distributed spe-
cies in the genus. It is characterized by its usually
erect or slightly arching (non-cymbiform) spathe,
which differentiates into a proximal tube and distal
lamina (blade), with the translucent area of the in-
ner spathe surface 1.5 to 3 times longer than the
spadix, and by having the rachises of the leaf
blades usually naked.

Dracontium carderi, D. costaricense, D. loretense,

D. ornatum, and D. trianae are synonymized here
for the first time. The differences among the type
specimens are slight. They closely resemble each
other and the type of D. spruceanum, especially in
spathe shape and peduncle length

Dracontium spruceanum was first described by
Schott (1858b) as Echidnium spruceanum in honor
of Richard Spruce, who collected the holotype
(Spruce 2406, К) at São Gabriel along the Rio Ne-
gro in Amazonas, Brazil. This name was later trans-
ferred to the genus Cyrtosperma by Engler (1878),
and subsequently not considered to be a Dracon-
пит based on Englers inference of a unilocular
ovary. This is a misinterpretation, since anatomical
study indicates that the specimen is too young to
vield accurate information (Richard Keating, pers.

comm.). Further, specimens collected near the type

—

locality usually have a single ovule in each of two
or three locules per ovary.

Dracontium spruceanum shares a long peduncle
with D. asperispathum, D. croatii, D. grandispa-
thum, D. longipes, D. peruvianum, D. pittieri, and
D. plowmanú. Dracontium croatit, D. pittieri, and
D. peruvianum differ in having a cymbiform spathe
that is not differentiated into a proximal tube and
a distal lamina, whereas the others listed above
have a non-cymbiform spathe that is constricted at
the base to form a proximal tube and distal lamina.
Dracontium plowmanii differs from D. spruceanum
(as well as D. asperispathum and D. grandispathum)
in having smaller seeds with a single dorsal ridge
and a spathe usually wrinkled along the margins.
Dracontium asperispathum also differs from D.
spruceanum in having the inner spathe surface
densely covered with translucent scales (vs. the in-
ner spathe surface semiglossy in D. spruceanum).
Finally, D. grandispathum differs from D. sprucean-
um in having a much larger spathe that is abruptly
acuminate at the apex (45—50 em long and 10—15
em wide vs. 20-35 cm long and 3-6 em wide and
gradually acuminate for D. spruceanum).

Additional specimens examined. BRAZIL. l1
as: basin of Rio Purus, s к on Rio Cunhuá at C:
ahuá, Prance et al. 16400 (INPA, NY, U, US); Benjamim
Constant, Alto Solimões, Ta 6909 (MO. RB); Manaus
km 18 da BR-17, Luiz 2996 (INPA, MG); Río Solimões.
Tonantins, Froes 12233 (NY). COI OMBIA Caquetá, San
Vicente del Caguán. Neiva-San Vicente, Betancur et al.
1874 (COL). Amazonas: Río ro 2 km downriver
from Puerto Nariño. Plowman et al. 2412 (COL, ECON
GH); Mun. Leticia, PN
(MO). Antioquia: Mace
cela de don Cipriano, Quebrada “Guarda sol,”

. 7738 (HUA, K, MO, ; Corr. Providencia, above
hydroe Чесите plant, gena & Villa 2750 (GH); Par. Nac.
Nat. “Las Orquídeas,” Cogollo et al. 4063 (JAUM), Co-

gollo et al 3583 (J. NIY ) 2 km S of Chigorodó, Haught

662

Annals of the
Missouri Botanical Garden

4585 (COL); San I ufs, Cañón del Río Claro, Cogollo et
al. 1455 (JAUM); Segovia, km 15 via Zaragoza Cerro Ca-
bezas, Rfo Pocuné, Cb et al. 52 (COL). Chocó: Bo-
lívar-Quibdó, km 67, Grayum et al. 7638 (MO); Alto 55
Baudó, Resguardo Indíge na Emberá, La Rotta 586 (COL);
La Mojarra, near Istmina, 9 оза 1307 (JAUM, МО); La
Archer 1729 (US); Pueblo Rico-Istmina,
Quebrada Antón, 15 km W of Santa Cecilia, Croat 70886
(MO, TULV); Quibdó-Río Atrato, /drobo & Cuatrecasas
2685 (COL); Río и е of Rio San ers For-
ero et al. 4823 (COL). : Honoria, Bosque Nac. Iparia,
toward El Parrao, sk "I775 (Е); Río Duda near the
mouth of Río Guayabero, Pérez 7191 (COL); qua de
San Martín, Madison 848 (GH); La Serranía, Río Ariari at
Aguasucia Lake, Jaramillo 1036 (COL); Río Guatiquia,
André 1025 (K); Sabanas de San Juan de Arama, Rfo Ghe-
jar, near Los Micos airport, /drobo 1193 (COL); Sierra de
a Macarena, Сайо E pim. ш 2203 (COL); NE
JS), Triana 289 (BM). N

Albi. М. S. Gon-
, Cuasambf, M.

vicencio, Cuatrecasas 463.
rino: Fumaco, re 5 indige na Alto A
zález 125 (COL); Tumaco, Llorente,
S. González 13 (( o Santander: , Cerro de
Armas, 70 km N of Velez, Fassett nien 6 (NY, US); Puerto
Berrio, ag Ur 2203 (US) Barranca 1 Mi in
1575 . Valle: Cordillera Occidental, Río
Sqn La Laguna, Cuatrecasas 15697 p. юш
, Río Vaupés, bordi of Cerro de Мий, Zarucchi 1916A

, Schultes & Cabrera 17184 (GH):
Hío Piraparaná Cafio Teemeeña, Schultes & Cabrera
17184 (GH). COSTA RICA. Limón: BriBri on Hío Six-
aola, Río Catarata, Baker & Burger 111 (F, MO); Fila Car-
bón, 6 km E of Home Creek, Hammel et al. 18119 (C R):
Quebrada Mata de Limón, Grayum et al. 4461 (MO); E of
Puerto Viejo de Sarapiquí, Grayum 4417 (MO); 2 km S of
Manzanillo de Talamanca, Grayum et al. 4388 (MO); Res.
Indige па 1 ‘a, Amubri-Cachabri, Chacón 1 (MO);
abo ‚ of Río Urén Sukut,

3189 (C R). EC UADOR, Manabi: at. Park
near Puerto López, Gentry & Josse 7. py (MO). Napo: 8
1 E of Puerto Misahualy Hedin 144 (MO); Jatun Sacha,
Cerón 1046 (MO, QCNE); Limón Cocha, Madison et al.
5343 (SEL); Nueve Rocafuerte, Alarcon 62 (QCA); Reser-
va Faunistica Cuyabeno, Río Aguarico, Palacios et al.
7660 (QCNE); Río Arajuno, Sola Cocha, Neill et al. 6978
(F, MO, QCA); 6 km NNW of Ahuano, Kohn 1193 (MO,
WIS); Añangu, Lawesson et al. 39334 we 2 José de

Payamino, 40 km W of Coca, /rvine et al. 968 (F); Res.
col. Antisana, Shamato, J. L. Clark et al. pr (MO,
QCNE); Hollín-Loreto, N of Ar mE Whitten et al.

93091 (MO); Río Shiripuno, Huantime, J. 5. Miller & P.
Yépez, Bai 562 (QCA); Laguna Limoncocha, Jaramillo &
Grijalv E 11555 (QCA); Chiro Isla, Río Napo, А. Bensmab
189 (QCA). Pastaza: Lorocachi, С km om Río Curaray,
pudo et al. 30780 (AAU, MO); S of Río Curaray,
mouth of Río Querano, Ape & nd ‘ios 6760 (MO); Mera,
Plowman 4490 (G ) km S of Puyo, Croat 50533
(MO, QCA). Sue se camels Gonzalo Pizarro, 8
km SW of Recinto Amazonas, Yánez & Shuigra 854
(QCA). VVV between La Saquea and Ya-
cuambf, 1 km N of Chapintza, Harling & Andersson 23856
(GB); Pachicutza, trail to Hito, Palacios et al. 8309 (MO).

NAMA. Bocas del Toro: trail to Quebrada Rabo de
uerco, Santamaría et al. 803 (PMA); Santa Rosa on Río
1503 (MO). Coclé: Distrito Ola, Po-
trero Шао Колево via La Pintada and Llano Grande,
‚ 2000, Guerra & Wong 1036 (PMA); Alto Calvario,
5-7 з N of El Cope, Thompson 4733 (CM). Colón:

—
—
>
—
—

Guasimo, Croat 9925 (MO); Santa Rita n Croat
О). Darién: upper Río Tuquesa, Clezio 25 (МО).
Panamá: Campo Tres, 3 mi. NE of Altos de Pacora, Croat
22756 (MO); Altos de Pacora NE of Cerro Azul, Dressler
(PMA); Cerro Jefe area, Dressler 3397 (PMA);
Parque Nacional Altos de Campana, Serrania del Llorón,
Galdames et al. 4382 (PMA); El Llano—Cartf Rd., mi. 6-
10, Churchill 3824 (MO). San Blas: vic. Cangandí, de
Nevers & Бана 5668 (MO): Cerro Brewster, de Nevers et
al. 6283 (MO); El Llano-Cartí rd., Nusagandf, G. Zhu
1504 (MO); Sw of к arto Obaldfa, Croat 16799 (MO).
Veraguas: Santa Fe area, N Alto de Piedra, Croat 23126
(MO). PE RU. кыы: Río na о 1327
(МО); СаШеа, Rfo Santiago, 3 3579 (MO); Quebrada
Caterpiza, Río Santiago, 05 N of Pinglo, Huashikat

428 (MO); pes Cenepa, Ancuash 129, 164 (MO); Huam-
pami, ca. 5 km E of Chávez Valdivia, Ancuash 1415 (MO).
Loreto: жч Mpa yo, Vdsquez 15226 (MO); An-

doas, Vásquez 3005 (MO); Yanamono Exp. Camp, 50 km
y river from Iquitos, J. P. Ti din & M. C. Hedin 107
(MO); Río Momon, trib. of Río Nanay, near Iquitos, Gus-
tafson 1972 (MO); Pto
; San Antonio,
(MO); Río Macusari, McDaniel 11018 ( SURIN ч
Nickerie: Nabij Kamp Koewinikreek, Elias 17. 317 (BBS).
VENEZUELA. Amazonas: | km S of San Carlos de Río
Negro, Liesner 9047 (MO, des N

Cultivated plants. Cult. Great Britain, Chelsea, Wil-
liam Bulls, Carder s.n. (K). Ecuador. Napo, Limón Cocha,
240 m, coll. by Madison, Plowman, and Besse, cult. at
Kew (162-80-1627), from Selby 1978-2038, Mayo 130

К); Napo, cult. at MBG, from Selby 76-95-4, б. Zhu
1499, 1490 (MO); Coca, 0°28'S, 76%58'W, cult. by В.
Feuerstein, Croat 75574, 75402; G. Zhu 1494, 1511

(MO); Limón Cocha, cult. at MBG, from Selby 78- A
G. Zhu 1448, 1486 (MO); Morona-Santiago, cult. by Betsy
Feuerstein, vouchered as Croat 78393 (MO); Zamora-
Chinchipe, Pn hicutza, 900 m, coll. by Henk van der
Werff, Mar. 1994, G. Zhu 1492 (MO); Pastaza, Mera, cult.
t Selby ( Shri ns (95-76-14), yis man 4490 (SEL), Chris-
tenson 1102 (SEL), Cobb 45 (SEL). Madison 4176
not seen); Esmeraldas, 10 mi. N ul Lita in July 1989, coll.
by Morell, Hyndeman & Fisk, from J. Boos (West Palm
Beach, Florida), cult. at Dewey Fisk's, Davie, Florida, G.
Zhu 1443 (MO)

pu
ur
т]
—

23. Dracontium ulei K. Krause, Notizbl. Bot.
Gart. Berlin-Dahlem 6: 115. 1914. TYPE:
Brazil. Acre: near Sao Francisco & Alto Xap-
игу, Oct. 1911, Z. Ule 9215 Um B!; iso-
types, В not seen, K). Figure

Tuber hemispherical or rarely rounded, 6-12 cm
diam., 6-9 em thick, flat above, rounded, white to
brown below, 8-20 cm below ground level; tubercles
few, rounded or cylindrically elongated, 0.5-1 X 1-
1.5 em, borne around the periphery of tuber; roots
white, sometimes tinged pink above the tuber, to 2.5
mm diam.; cataphylls 1 (concealed from view soon
after leaf development), 10-20 cm long, 1-2 cm
wide, light brown, reaching or surpassing ground
level. Leaves solitary; petioles 1-1.2 m long above
ground. 2—4 ст diam. at midpoint, dark green tinged

Volume 91, Number 4 Zhu & Croat 663
2004 Revision of Dracontium

0.5 cm

A A
Figure 27. A-D, Dracontium ulei. —A. Two separate inflorescences, one in face view, one cut into two halves (Nee
31734). —B. Two infructescences with base » pe tiole, the inflorescence on the right with the spathe still persistent,
the one on the left with lange ning berries. —C. Leaf showing the three divisions of the blade (Croat 85115). —D.
Seeds in lateral view (Ule 9215).

664

Annals of the
Missouri Botanical Garden

brown, contrastingly mottled with dirty white or pale
green blotches and forming a reptilian pattern, usu-
ally smooth in upper half and with irregular protu-
berances in lower half; juvenile blade sagittate, or
sagittately lobed; mature blades ascending to 45°

the petiole (often), 0,8—1 m diam.,
rarely fenestrate, never variegated, with abundant
raphide cells and often dark markings, glossy and
medium green above, glossy and dark green below;
8 division twice trichotomously branched, 50—
60 X 50-55 em, with terminal subdivision consist-

papyraceous,

ing af 3 sections, with each basal subdivision con-
sisting of many segments; lateral divisions twice
dichotomously branched, 50-65 х 55—60 cm, with
terminal subdivision consisting of 2 sections, with
basal subdivision consisting of many segments; ter-
minal and subterminal sections free; leaf segments
often entire, broadly oblanceolate, more than 5 cm
wide on each side of the major ribs, oblanceolate,
mostly free from each other in each division, often
with contrastingly smaller rounded or triangular seg-
ments alternating with larger segments; apices acu-
minate; ultimate segments 10-15 cm long, often free
from penultimate segments; other segments 3-8 cm
long; penultimate segments free from subterminal
sections; medial segments free from basal subdivi-
sions; basal segments present, free from each other;
rachises patterned distinct from petiole, pale green,
tertiary veins obscure above and weakly
raised below; bracteoles 2 or З, 820 X 1-2 cm,
pink, the longest one + as long as the peduncle,
reaching the spathe. /nflorescence solitary, appearing
before new leaf; peduncle 8-20 cm long above
ground, 0.6-0.8 em diam. at midpoint, often almost
completely subterranean, scarcely mottled, whitish
tinged pink, smooth; spathe 6-10 cm long, 34 cm

smooth;

wide, non-cymbiform, constricted at a certain point
and differentiated into a proximal tube and a distal
lamina (blade), cucullate, arching 457—907, apex
acuminate; 4-6 X 34 cm at widest point; lamina
shorter than the tube; inner surface covered with
dense, translucent scales to 1 mm long, violet-pur-
ple, with translucent area obscure; outer surface ma-
roon tinged brown, matte; margins entire, broadly
overlapping in the lower two-thirds; veins obscure
inside and outside, similar to the spathe in color;
spadix hidden, stipitate, cylindric, brown-purple, 3—
4 em long, 1.2-1.4 em diam. at anthesis, never with
appendages at apex; stipe 0.4-0.5 cm long, 0.5 cm
diam. at anthesis. Flower tepals 4 to 6, 2-3 mm long,
1-1.5 mm wide, light brown; stamens 4 to 6: fila-
ments 1.5—4 mm long; anthers 0.8 mm long (elliptic).
completely exserted; ovary incompletely 3- or 4-loc-
ular, white: 4-lobed; style 1-1.5 mm
long above tepals, brownish purple, persistent. /n-

stigma 3- or

fructescence with spadix 6-7(-10) em long, 1.5-2(-

3) em diam. in fruit; berries 2-seeded, young berries
0.4—0.5 em diam., 0.5-0.7 cm thick, obliquely ob-
ovoid, apically subtruncate; young berries medium
green; mature berries color unknown, with abundant
raphide cells; seeds 0.4—0.5
dish brown, laterally raised, smooth; dorsal ridges

cm diam., reniform, red-

obscure.
Phenology. Flowering in early September;

young infructescences collected in October and

mature fruits in October.
Distribution and habitat. Dracontium ulei rang-

es from Acre, Brazil, to Pando, Bolivia. It occurs
in the Tropical moist forest (T-mf) life zone (Hold-
1971), at 125-230 m.

*Milho de cobra"

ridge et al.,
Local names.

592, NY).
Discussion.

its usually subterranean peduncle and inner sur-

(Lowrie et al.
Dracontium ulei is characterized by

face of the spathe densely covered with translucent
scales. It is easily confused with D. bogneri, which
shares a cucullate spathe covered inside with trans-
lucent scales. However, D. bogneri has seeds lat-
erally depressed with 3 obvious dorsal ridges (vs.
aterally raised. with obscure dorsal ridges for D.
ulei). Dracontium ulei is also close to D. dubium
and D. purdieanum, but can be distinguished by its
spadix concealed at anthesis and deeply hooded
spathe with small scales to | mm long on the inner
surface. The latter two species differ by having the
spadix exposed at anthesis and a spathe that is not
hooded and lacks scales this small on the inner

surface.

BOLIVIA. Pando:
4 (MO, NY). BRAZIL.
in 110 Nelson 752 (MG, MO,
;aete, — et al. 7925
(NY, US); Rio e 0- Xapury, BR ‚ km 16, Cid &
а 2987 MG, МО); К : Wels na Madureira, 3i
Cid & Souza 3022 (N s Brasil, basin of Ri
А urus, upper Rio Acre, is et T 9820 (N Y).

Additional specimens e
Río Madre de Dios, Sena,
Acre: Rio Вгапс‹ o- аи
К); Rio ( above mouth,

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)ne new name and five new combinations
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in i 5 73—7

— ——— & D. H. Nicolson. 1991. A dd ación ation
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Croat, T. B. 1975 E new species of Dracontium (Aracea
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3e

Novon 5: 30
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8 )

Ara-

—

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Identity and

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Novon 8:

—

APPENDIX 1. List of species.

. Dracontium amazonense G. Zhu & Croat
> Dracontium — G. Zhu & Croat
3. Dracontium asperispath >. Zhu & Croat
4. Dracontium asperum К. < ch
5. Dracontium ddp С. Zhu & Croat
6. Dracontium croatii G. Zhu
7. Dracontium dubium Kunth
8. Dracontium gigas (Seem.) Eng
9. Dracontium grandispathum G. Zhu & Croat

10. Dracontium grayumia inum G. Zhu & Croat
11. Dracontium guianense G. Zhu & Croat

12. Dracontium longipes Engl.

13. Dracontium margaretae Bogner

. Dracontium peruvianum G. Zhu & Croat

. Dracontium pittieri Engl.

17. Dracontium plowmanii G. Zhu & Croal
. Dracontium polyphyllum

. Dracontium prancei G. Zhu & Croat

. Dracontium purdieanum (Schott) Engl.
Dracontium soconuscum Matuda

. Dracontium bs ond = hott) G. Zhu
. Dracontium ulei К.
APPENDIX 2. Index to exsiccatae. Type species in
boldface.

R. Aguilar 1976 (16); R. Aguilar € V. Guzmán 2849
(16); Alarcon 62 (22); P. Alcorn & J. Mallet 8 (15); P.
Allen 3427 (21), 5318 (16); Alson 971 (18), 1107 (18);
E. Ancuash 129 (22), 164 (22), 1415 (22); André 1025
(22); ä s.n. 1. in 1889 (8), s.n. (8); Т. Antonio 3736
(22); Archer 172¢ ; Aristeguieta 5381 (7), 12734 (7).
s.n. (20); viria 19281 (22), 14 2588 (22); M. Aulestia
gc )); Aymard & recs 3807

Jaker & Burger 111 (22); Balée 2106 (18), 3476 (14);
P iol 5817 Ts A. Barfod ies 597 (6); Barnes s.n.

er
=
—

(4), 4 (4); Barret s.n. (4); Bartlett & Lasser 1683
(21); а һ 1490 (8); К. ш 189 (22); Betancur
et al. 1874 (22); Berlin 2034 (22), 3579 (22); С. Black

47-2084 (14), 18814 (14); Bogner s.n. (2), s.n. ‚11:
(19), 1267 (8), 2097 (5); Boos s.n. (TRIN 31296) (4);
Bosbeheer 9845 (18); Britton & Britton 10060 (4); Broad-
way 407 (18), 5212 (4), 7 py ). 7926 (4), 9214 (4); N.
E. Brown s.n. in 1878 (8). в 8), s.n. in 1881 (8), s.n.
in 1883 (8); W. ey s.n. (8); Bunting 2856 (7), 3677A (7).
2 (7); Bunting & Trujillo 2221 (7), 2222
(7), 2225 (7); Bunting et al. 10866
(20); Burger 8 Baker 9999 (8),
Gentry 9017 (16); Burger & Stolze 5551 (16). 580
5845 (8), 9017 (16); Burger et al. 10587 (16), 12266A
(16), 12266B (16).

Callejas et al. 4166 (22); Е a 1805 (10); cid
er s.n. (22); ( ET et al. 53 (22); Castillo 260 (7);
Catharino et al. (13); eem 1046 (22), 3598 rs

wa
—
N
N
N
—
5 =
—
oe
N
NN
= =

Сегбп > M. e ón m (9), 4687 (22); Chacón 1 (22).
1414 (21); Christenson 1102 e 1154 (6), 1287 (17),
1490 (17), 1491 (17), 1576 (6); Н. W. Churchill 3824 (22);

Cid & Souza 2987 (23), 2988 2 3). 3022 (23); J. L. Clark
et al. 5014 (22); Clezio 25 (22); Cobb 45 (22); Cogollo et
al. 1455 (22), 1497 (22), 1524 (22), 3583 (22), 4063 (22
Cornejo 1520 (17); Cowan 38843 (18); Cremers 7682 (18
11618 (18), 12734 (18), 12737 (18); Cremers & Crozie
14308 (18); T. B. Croat 9925 (22), 12246 Qu. 16700 (22),
17986 (22), 19391 (3), 20550 (3), 22756 (22), 23126 (22),
27217 (22), 27794 (21), 27795 (21), жеч» (22), 3:
(16), 36370 (8), 50533 (22), 53539 (15), 53561 (1), 56898
(1), 62349 (12), 68381 (8), 70886 (22). 71785 (18),
(6). 71840 (8). 71895 (1), 72308 (6). 73040 (6). 73867
(19), 73989 (17), 74210 (18), 74284 (18), 75402 (22).
75574 (22). 78393 (22). зк (23), 85460 (12); T. B.
Croat & P ae 59844. (16); T. B. Croat & D. Hannon
79217 ee = 4633 (22), 15697 (22), 16474
ао; Anc 349

Jaly et al. 9820 p^ 3). 10000 (12); Davidson 8624 (8):

nu on & Jones 9605 (1); Delascio 6818 (7)
ward 67 (18), 88 (18); A. T. G. Dias 513 (18); C.
al. 1164 (3 W. Dodge 5622 (8); Dodson 5951 (6)
7288 (6); Dodson & Fallen 7762 (6); Dodson et =
; Dressler s.n. (21), 3397 (22),
4608 (22); Duarte 6909 (2: 2) 1 1161

(20); J. Duke ! 5103 (10).

Volume 91, Number 4 Zhu & Croat 667
2004 Revision of Dracontium

о cane (18): Elias 17317 (22); Emmerich 4053 С. de Nevers & H. Herrera 5668 (22); G. de Nevers et
(13), : al. 6283 (22); сне 1119 (18): P. Nuñez 1885 (17).

о P E 5( Y 4249 (21); Fassett 25426 (22); Feuillet
3993 (18): Fleury 802 (18); Florschutz & Maas 3162 (4):
Foldats 216A (7): Folsom 4583 (10), 5740 (22); Forero el
al. 3800 (10), 4718 (10), 4823 (22); R. B. Foster 1724
(22). 4389 (2), 6978 (12). 7212 (17), 9558 (17); Foster et

al. ida ): Froes us 22).

raldames et al.“ ; Garcia et al. 1527 (21):
Еа 1639A (21); sa 60 (18). 234 (14); Gentry 2598
21) Ge i) & Daly 18798 (15); Gentry & L. F
38721 (3): Gentry & C. Josse 72402 (22); Gentry & Р.
Nines gi 3 (17); Gentry & Ortiz 74202 (3); Gentry et
5), 29076 (3), 30026 (15), 37215 (3), 42629
(3), 51 147 A 52159 (15), 54686 (3), 78072 (17); Ginz-
berger s.n. (16), 3109 (14); Girardi 16 (7); Gómez 18513
(8). 22029 (16). 22935 (16); E. p rer 97 (13); Gon-
zález 13 (22); Gragson & Gragson 4 (13), 1 dis 3k C.
dez et al. 2629 (15); de Granville & Cre

1); Grayum 7992 (8), 7911 (8); Grayum al ri
(22), 4461 (22), 6046 (16), 7638 (22); Grenand 1277 (1 1),
1913 (18); C. Guerra & B. Wong 1036 (22

Hahn et al. 17 (2); Hallé 790 (18); Hammel 11764 (8);
Hammel & D'Arcy 6364 (22); Hammel & Wilder 17283
9); Hammel et al. 15204 (16), 18119 (22); Harling &
Andersson 16404 (9), 23856 (22); Hassler 10960 (13):
en 1575 (22), 1741 (22), 2203 (22) 4585 (22); Hax-

e 1757 (2), 2877 (2); J. 1 7 8 144 (22): Herrera 252A
(10), 3189 (22), 4529 (16); W. S. Hoover et al. 3279 (6);
Moyos & Hernandez 241 (2: 2): Huber 1826 (7), 1826-1
(7), 2036 (14), 3667 (14); Huashikat 428 (22).

Idrobo 1193 (22); Idrobo & Cuatrecasas 2685 (22); In-
chaustegui s.n. СЕ rvine et al. 968 (22); Irwin 55045
4); Irwin et al. 30 (5), 55749 (4).

5 oe on 3598 (22), 4938 (22); Jaramillo et
al. 30780 (22): Jácome 399 (22); Jacquemin 2191 (18),
2194 (18); d 491 (4). 6895 (4); Jimenez 3420 (4);
Jipa et al. ; Johnson 243 (4); de Jong 20 (15);
Junc оза Tes 1255
alloo & Gonzales 1358 (4); Kastelein 16153 (18); R.
5 (22), 1327 (22): Ke Rie 1646 (16); C. Kernan

& P. ae к; (16); Killip & Smith 29351 (2); Kin
11 | 4 (2); Knapp У Mallet 7210 (15); Кос h
s.n. (4); Kohn gi (22). 1210 (22); Kress 76585 (16)
Krukoff 4987 (15); Kugikat 1132 (16).

La oy 586 (22); Larpin 998 (18); J. E. Lawesson et
al. 39334. (22); i god н 9 (8); ee s.n. ee
E ue 1222 bo

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. ‚ 530 (2: 3), 5 2 (23); L vow 3301 (21),
‚ 16831(21); Luteyn et E 9021 (9); Luiz 2996 (22)

; P. J. M. ! . 8299 (1),
(12); Machiel & Rosário 534 (14); Madison 848 (22), 3764
(21), 4140 (6), 4176 (22). 4229 (17); Madison et al. 5343
22); Marín 285 (16); Martin & Lau-Cam 1315 (2 ); Mar-
tinelli et al. 6815 (18); Martius 282 (14); Matuda 17780
21); Mayo 130 (22); McAlpin 85-34 (16); McDaniel
11018 (23); Meier 435 (7); Milliken 1717 (4); Milliken et
al. 511 (19); J. К. Morales 546 (16); Moretti 122 (18); Mori
E (22); Mori & Kallunki 2590 (22); Mori et al. 9666

18).

Nee 31734 (23); D. he LI (8), 8713 (22); D. Neill
& W. Palacios 6760 (22 eill & Vincelli 3512 (8);
D. Neill et al. 6978 (22). M (3); С. Nelson 752 (23);

5

e 748 (7); Ortega & VENE UEM ta 15

Palacios 1654 (22), 4242 (9) - Palaei ‘ios et al.
31 1 (9). 7660 (22), 8309 (22); Paris т (18); Pérez 7191
(22); Pesha 5 (17); Philipson 2203 (22): Pinkley 60 (9);
Pipoly 15612 (3); Pipoly et al. 12535 (3), 13282 (3); J.
M. Pires 6594. (14); Pittier 1775 (22), 3429 (21), 3650
(21), 4232 (22), 1 (10), 9232 (22), 11985 (16): Piitier
& Tonduz 7515 (16); Plowman 4490 (22), 10926 (6),
12043 (5); е & Davis 4490 (22), 5054 (17), 5054
17): Plowman & Kennedy 5654 (17): -— man & Martin
1661 (3); Plowman & Schunke V. 11536 (15): deum
el al. 2412 (22), 6720 (2), 6728 (3), 6729 (3), 6815 (2).
6820 (3), 8616 (18), 9895 (14), 12510 (1), 12550 (1):
Proctor 46104 (4), se رو‎ (4), 47976 (4), 48044. (4), 48047
э (23), 16400 (22), 28732 (19);

(18); 5 in 1845 (20).

F. Quesada 259 (16

Re nterfa 4220 (10); Tal & Cardenas 4314 (10);
Renterfa et al. 4212 (10); Richard s.n. (18); Riera 415
(1 8); Wm hi 4043 (15), 5304 (15); ame 158 (7):
1 (8); R. ery 6357 (10); Rudas et al. : тере
2869 (8), 3295 (8), 3390 (8), fon 8).

8615 (8), 10190 m
Sagot 608 А Salick 7370 (15); Sang 16866 (18); San-
{атага et al. 803 (22); у rs 1920 (4); Sauvain 175
(18); Schultes qu (2); Schultes & Cabrera 17184 (22);
Schultze-Rhonhof 2998 (22), 3031 (22); Schunke-Vigo
"uo P2 6428 (15), 7140 (15); Shank & Molina 4953
( „ Smith 3029 (4); Soejarto & Villa 2750 (22); J.
Solomon 5334 (8); Spruce 2406 (22); Stahel s.n. (18);
ndley & Valerio 48885 (8), 49002 (8); B. Stein et al.
» (2) т» & Delgado 12940 (18); Stern et al. 93
(10); . Stevens 7007 ( y |
8 et al. 117171 (7), 127097 (7), 131647 (1):
Strudwick et al. 3987 (18); Susach 251 (13); Sytsma et al.
(22).

^^
—

4269
Tamayo 3188 (1); e 4658 (5) 1686 (22).
e ds 4821 (22); 1. Thurn s.n. (4); Tina & Tello 2054
y & Alcorn 198 (2); Triana 280 22), 691 (22):
3 (13).

—

(3);
iii 1263:
2), B

—

1). 5781 (12), 9215 (23);

p 24 (8), 678 e Vargas 13433 (17); R. Vás-
z & М. Jaramillo 3598 ü 5). 4938 (2), 7595 (2), 8562
(15). 15226 (15), 16094 (3), 16524 (2); R. Vásquez et
al. 3005 (22), 4838 (2), 4841 (17). 6761 (2), 8081 (2).
Whitten et al. 93091 (22); Williams 155 (3), 827 (2).
1750 (3), 1942 (3), 2119 (3), 3756 (2), 4631 (15), 5144
(22), 7916 (15); Woodbury s.n. (4); Wullschlaegel 1096
(4); bones k ee Monachino 41392 (7).
A. & Shuigra 854 (22); R. Young 189 (17
2 1459 (22), 1916A (22); С. Z
(8), 1156 (8), 1157 (8),

1456 (1), 1457 (1), 1458 (1‹ 9), `1459 (б),
(1), 1462 (18), 1463 (19), 1464 (1), 1465 (1), 1466 (17),
1467 (8), 1478 (4), 1479 (4), 1480 (17), 1481 (8),
(17), 1483 (18), 1484 (4), 1485 (21). 1486 (22), 1487 (17).

1489 (1), 1490 (22), 1492 (22),
(17). 1496A (17),
1498 (17), 1499 (22), 1501 (19), 1509 (4), 1510 (5),
(22), 1512 (17), 1513 (18), 1514 (1), 1515 (4),
7 (8), 1518 (6), 1533 (13), 1580 (6); G. Zhu € T. B.
Croat 1503 (22), 1502 с 1504 (22), 1506 ( 10), 1507
(10); G. Zhu et al. 1505

REVISION OF Thomas В. Croat?
DIEFFENBACHIA (ARACEAE)

OF MEXICO, CENTRAL

AMERICA, AND THE WEST

INDIES!

ABSTRACT

The genus Dieffenbachia Schott has approximately 135 species, most of them occurring in South America. Major
centers of diversity for the ge p inc a Colombia with 37 spec ies, d uador f vise Peru (30), Brazil (27), Panama (20),
and Costa Rica (13). There are 26 species in Central America, with 20 species (77%) new to science. These are :
burgeri Croat а Grayum, D. copensis C bs D. crebripistillata Croat, . D. davidsei Croat & Grayum, D. fo Loita roa
osteri Croat, D. galdamesiae Croat, D. horichii Croat & Grayum, D. isthmia Croat, D. killipii Croat, D. lutheri C roat,

). pata Croat, D. obse 'urinervia Croat, D. panamensis Croat, and D. standleyi Croat described herein and
» 'achiana. Croat & Grayum, D. concinna Croat & Grayum, D. grayumii Croat, D. hammelii Croat € Grayum, and p
tonduzii Croat $ Grayum dese iibe di e en here. Most species range from Nicaragua to Panama. Belize has only 1 a ies
of Dieffenbachia; Mexico, El Salvador, and Guatemala have 2 s spec ies, followed by Honduras (3), Nicaragua (6), Costa
Rica (13), and Panama (20). Only a few Central American species could be e considered widespread. Among the most
widespreat id are D. oerstedii Schott and D. wendlandii Schott, both of which range from Mexico to Panama, as well a

D. nitidipetiolata and D. tonduzii, which range from Honduras to Ecu ador. Species destin : high. especially in
Coli Rica (3) and Panama (9). A total of 9 species are shared between P anama and Costa Ri dos species, almost
31% - the = жын into South America. These are D. davidsei, D. isthmia, D. killipii, D. рема D. nitidipe-
tiolata, D. ‚ D. seguine, and D. tonduzti. Most of these only exte nd to Colombia, but three species,

Шр, D. „ and D. tonduzii, range to Ecuador. Only D. 1 8 ranges to the eastern slope of the Andes.
us i ipn hia seguine ranges into Brazil and Bolivia, from the West In die
yrds: Araceae, Central America, Dieffenbachia, Mexico, South ran rica, West Indies.

The family Araceae is worldwide in distribution. Schott ex K. Krause). Important local centers of
but most species occur in tropical areas. Its centers generic endemism in the family include Brazil,
of distribution include both Asia and America which has four endemic genera (Bognera Mayo €
(Croat, 1979), with 31 genera in the Americas and Nicolson, Dracontioides Engl., Gearum N. E. Br.,
28 found in Asia. There are 16 genera in Africa. Zomicarpa Schott), and the Indomalaysian region,
Madagascar, and the Seychelles. A few genera are with 14 endemic genera. At least 2550 species,
o temperate regions of the Northern representing four-fifths of the total, occur in the

restricted
Hemisphere, including the Mediterranean region Neotropics. The Central. American flora comprises
(Calla L., Lysichiton Schott, Orontium L., Peltandra 19 genera within the Araceae.

Raf., Symplocarpus Salisb. ex Nutt.), including the With an estimate of more than 2550 species in
Mediterranean region (Arisarum Mill., Ambrosina Latin America, the Araceae are one of the largest
Bassi. Arum L.. Dracunculus Mill., Helicodiceros families of flowering plants in the region. Yet no

I This revision could not have been completed without the ёзу ated and able assistance of my former co-worker,
Petra Schmidt, who partic ipated in nearly every phase of the work. She continued the researc +h efforts unabated while
| was in the field. Monica Carlsen and К mily т. former 1 present Research Assistants, respectively, were re-
sponsible for final editing and revision of the manuse nipi including final preparation of legend images. Fred K eusen-
kothen was responsible for preparation of scanned images. Special thanks also must go to Ch егу! Neuman and F
Colletti, Research Greenhouse managers during the course of this work, who mainisined hundreds к Diefenbach
collections in healthy a eek: Very spec em thanks also go to my colleague and fellow aroid specialist Mike Grayum,

whose knowledge of the Costa Rican da eae is unparalleled. Dan Nicolson, from the U.S. National He danaa: pu
Charlotte Taylor, MO, assisted with nomenclatural issues. John Rawlins, from the Carnegie Museum, Pittsburgh, de-
termined most of the о collected for this revision of Dieffenbachia. Thanks also go to Helen Young for beetle
determinations and for 5 on re p tive biology. Elenor Sauer has proofread or written Latin diagnoses for
all of the new species. Her expert assistance is greatly appreciated. Finally, | would | like to thank my wife, Patricia,
who has put up with my long aa nces while donk fieldwork for more than three decades. She was always available

—

us an juu and to solve computer and database prob ems
? P. A, Schulze, Curator of Botany, Missouri Botanical Garde in, PO. Box 299, St. Louis, Missouri 63166-0299, U.S.A.

ANN. Missourt Bor. GARD. 91: 668-772. 2004.

Volume 91, Number 4
2004

Croat 669
Revision of Dieffenbachia

other family is so poorly known taxonomically.
Plants exhibit considerable morphological plasticity
at all stages of development. Many of the genera,
especially the hemiepiphytic genera Rhodospatha
Poepp., Monstera Adans., and Syngonium Schott,

exhibit complex patterns of heterophylly, with dras-

tically different morphology at different stages of
development (Croat, 1981 [1982]; Ray. 1981,

1987).
parts, making them difficult to collect and preserve.

Most members of the family have succulent

Dieffenbachia is one of several medium-sized
genera in the Araceae, with an estimated 135 spe-
cies. This revision is the first major review of Dief-
fenbachia for Central America since Adolf Engler's
(1915)

Dieffenbachia is one of the most important genera

generic treatment in Das Pflanzenreich.
of understory herbs in the family, and it is often a
dominant component of humid to wet tropical for-
ests, especially from sea level to 1500 m. It inhab-
its life zones ranging through Premontane moist for-
est (P-mf), Tropical moist forest (T-mf), Premontane
wet forest (P-wf). Tropical wet forest (T-wf), and Pre-
montane rain forest (P-rf) (Holdridge, 1967). While
most species occur in virgin humid forests, the ge-
nus is known from freshwater swamps. stream
banks, regrowth forest, among rock outcrops, and
occasionally on road banks. It often constitutes the
most conspicuous element of the understory vege-
tation because of its abundance, frequent colonial
growth habit, and generally large, showy leaves.
The genus provides a wide variety of choice orna-
mental plants for horticulture, including most of the
species treated here.

The genus is distinct and not easily confused
with any other aroid. It is closest to Bognera, which
differs in lacking staminodia surrounding the pis-
tillate flowers and in having higher-order venation
reticulate. In contrast, Dieffenbachia has several
staminodia surrounding the pistils and higher-order
venation parallel-pinnate. However, the monotypic
genus Bognera is endemic to Brazil, and it is not
likely to be a problem with determination of most
Dieffenbachia. Alternatively, Dieffenbachia is fre-
quently confused with Philodendron Schott, partic-
ularly the terrestrial species of the latter with non-
cordate blades. Philodendron species are mostly
hemiepiphytic, rarely terrestrial as is Dieffenbachia.
Even when Philodendron species are terrestrial and
have non-cordate blades, they can be distinguished
by the remotely many-flowered pistils that are not

surrounded by staminodia, as well as the lack of

the acrid foul-smelling. irritating sap that is so
closely associated with Dieffenbachia.
Species diversity of Dieffenbachia shows a gen-

eral diminution from Mexico to Middle America

with the lowest totals just north of the San Juan
depression (Nicaragua), followed by a marked in-
crease approaching the South. American continent.
(In this treatment, Central America is defined as all
the area between Mexico and Colombia, whereas
Middle America is all the area between Mexico and
Panama.) Mexico has 2 species, Guatemala (2). Be-
lize (1). Honduras (3), El Salvador (2), Nicaragua
(6). Costa Rica (13), and Panama (20) (Table 1).
Endemism is high, especially in Costa Rica with 3
endemic species and Panama with 9. A total of 7
species are shared between Panama and Costa
Rica. Just under one-third (31%) of Central Amer-
ican species of Dieffenbachia range into South
America, isthmia, D.
killipii, D. longispatha, D. nitidipetiolata, D. obscu-
rinervia, D. seguine, and D. tonduzit.

these being D. davidsei,

MATERIALS AND METHODS

This revision is based on more than 29 years of
field. studies Central and South
tween 1967 and 1996. All but one species were

America, be-

studied live in the field or under cultivation at the
Missouri Botanical Garden. The descriptions have
been prepared from both living and dried. speci-
mens. The exception is D. fosteri, where the de-
scription was based solely on the type specimen.
The use of (“dried”) preceding all or any part of
the description is an indication that all that follows
is based on herbarium material only. Morphological
characters were coded directly into a computerized
database to ensure parallel and sortable descrip-
tions. The aroid descriptions database contains 784
character states applicable to the morphological di-
1997).

Discussions and references to illustrations, as well

versity expressed in Dieffenbachia (Croat.

as exsiccatae, are stored separately, but tied to a
particular species description and to the nomencla-
tural information by a unique taxon number. Ter-
minology and usage in the descriptions in this re-
vision are largely defined by Croat and Bunting
(1979) and elaborated in Croat (1997)

Ecological zones, though sometimes estimated
from my own experience with Central American
taken from Holdridge life-
1967; Holdridge et al.,

1971). where they exist for Central American coun-

vegetation, are largely

zone maps (Holdridge.

tries, and for Mexico from the "Mapa de tipos de
vegetación de la República de México” (Flores et
al, 7 71)

TAL material has been widely distributed
and original field vouchers are cited for all herbaria
whose material was seen (see Appendices l, 2).

Herbarium material may consist of one of three

670 Annals of the
Missouri Botanical Garden
Table 1. Distribution and endemism in A »nbachia species from Mexico, Central America and the West Indies.
X = spec ies present; E = endemic spec ies
Country
Gua- zol-
exi- te- S - Hon- cara- Costa West om- Ecua- Vene- Boliv-

Species co mala Belize pos duras gua Rica Panama Indies bia dor zuela Brazil ia
D. aurantiaca X X
D. beachiana X X
D. burgeri E
D. concinna X X
D. copensis E
D. crebripistillata [D
D. davidsei X X X
D. fortunensis E
D. fosteri E
D. galdamesiae E
D. grayumiana X X
D. hammelii E
D. hori E
D. нана X X
D. killipii X X X X
D. longispatha X X
D. lutheri E
D. nitidipetiolata X X X X X
D. obscurinervia X X
D. oerstedii X X X X X X X X
D. panamensis E
D. pittieri E
D. seguine X X X X X X
D. standleyi X X
D. tonduzii X X X X X
D. wendlandii X X X X X X X
Total number of 2 2 l 2 3 6 13 ) 8 1 1 1 l

species (percent (23%) (40%)

of endemics)

kinds: (1) complete original sets (wild collected);
(2) sterile original material with an inflorescence
added from a cultivated plant of the same number;
and (3) material collected entirely from the culti-
vated plant. Specimens based entirely or in part on
cultivated material are clearly indicated on the her-
barium label.
Herbarium specimens were oo from most
major he rbaria including: A, AAU, 5, А
A8, OCO, CM, COL, > А
DAV, . DUKE, EAP, ECON, ENCB, F, FLAS,
FSU, 118 dw H, GOET, GUAY, HBG, HUA, DD.

ISC, K. L, LA, LL, M, MEXU, MICH, MY, NY,
PMA, PORT, QAP. QCA, QCNE, RSA. S. SCZ.
SEL, STRI, TEFH, TEX, TULV, U, UC, UMO, US,

USC, USJ, VEN, and WIS. Unless specifically des-
ignated as not seen, all specimens are to be pre-
sumed to have been examined personally.

Data on the living collection of Dieffenbachia are

computerized, and the entire collection, including
many South American species that are being de-
scribed separately, undergoes regular inventories to
include events such as flowering time and attempt-
ed hybridizations. This allows electronic access to
information on status, location, flowering dates, the
number of vouchers prepared, and the status of the
description. All specimens cited have been record-
ed in a computerized database for permanent re-
ferral. See www.mobot.org.

HISTORY OF THE GENUS DIEFFENBACHIA

HEINRICH WILHELM SCHOTT

The genus Dieffenbachia was described in 1829
by Н. W. Schott (Schott, 1829). Schott based the
genus on a single species, Caladium seguinum
(Jacq.) Vent. (Ventenat, 1800), previously described
as Arum seguine Jacq. (Jacquin, 1763) as well as

Volume 91, Number 4 Croat 671
2004 Revision of Dieffenbachia

Table 2. Treatment of Dieffenbachia species by H.W. Schott (1860).

Species treated by Н. W. Schott (1860) Origin Synonymizations as treated by Engler (1915)

1. D. cognata Schott Suriname — D. seguine var. lineata (Mart. ex Schott) Engl.

2. D. consobrina Schott Brazil — D. seguine var. viridis Engl.

3. D. costata H. Karst. ex Schott Venezuela

4. D. gollmeriana Schott Venezuela — D. seguine var. viridis Engl.

5. D. humilis Poepp. Peru

6. D. irrorata Mart. ex Schott Brazil — D. seguine var. lingulata (Mart.) Engl. subvar.
irrorata (Mart.) Engl.

7. D. lineata K. Koch & Bouché New Granada — D. seguine var. lineata (K. Koch & Bouché)
Engl.

8. D. lingulata Mart. ex Schott Brazil — D. seguine var. lingulata (Mart. ex Schott) Engl.

9. D. liturata Schott Unknown — D. seguine var. liturata (Schott) Engl.

10. D. macrophylla Poepp. Peru

11. D. neglecta Schott Jamaica — D. seguine var. viridis Engl.

12. D. obliqua Poepp. dus

13. D. oerstedii Schott ‘entral America

14. D. picta Schott с nknov

15. D. plumieri Schott Martinique = D. seguine var. viridis Engl.

16. D. poeppigii Schott eru = D. seguine var. viridis Engl.

17. D. robusta Schott Unknown

18. D. seguine (Jacq.) Schott Martinique

19. D. spruceana Schott Brazil = D. humilis Poepp.

20. D. ventenatiana Schott Suriname = D. seguine var. ventenatiana (Schott) Engl.

21. D. wendlandii Schott El Salvador = D. seguine

by Linnaeus (1763). The next species described marum (Engler, 1879), 6 species were treated and
were three from Peru (Poeppig, 1845), D. humilis 2 more combinations were made. Between 1879
Poepp., D. macrophylla Poepp., and D. obliqua and 1899, 14 additional species were described,

Poepp. only 3 of which were recognized by Engler in 1915.
Between 1852 and 1864 an additional 18 spe- These were D. daguensis Engl., D. enderi Engl.,

cies were described, all but 4 of them by H. W. and D. olbia L. Linden & Rodigas.

Schott. Of these only 3 were recognized in Engler’s In 1899, Engler produced another small work on

(1915) revision, while the remainder were synony- Dieffenbachia in which he treated 19 species and

mized or recognized at the subspecific level, mostly made 24 new combinations, but provided no de-
under Dieffenbachia seguine. Those recognized at — scriptions except for one new species, Dieffenbach-
the specific level were D. picta Schott, D. costata id aurantiaca Engl. Only 9 species were described
Н. Karst. ex Schott, and D. oerstedii Schott. Be- between this work (1899) and Englers (1915) re-
tween 1866 and 1878, 12 species were described. vision. Those taxa still recognized by Engler (1915)
with 6 more of these being recognized as distinct were Dieffenbachia cordata. Engl., D. weberbaueri
Table 3). The first major re- Engl., D. gracilis Huber, and D. cannifolia Engl.

—

in Engler’s revision
vision of the genus was that of Schott (1860) in his ex Ule.

Prodromus Systematis Aroidearum, treating 21 spe- The last revision of the genus * was
cies, of which Engler later (1915) recognized only by Engler (1915) in Das Pflanzenreich. This revi-
7 (see Table 2). sion contained both keys and descriptions for 27

species. A total of 11 new combinations were made
ADOLF ENGLER and 6 new species described (see Table 3). The new
, 3 . v species were D. aglaonematifolia Engl., D. brittonii
The next revisionary effort made with Dieffen- ! Жы : if 8
Engl., D. longispatha Engl. & K. Krause, D. par-
bachia was by Engler (1878) in the treatment of the 5 си,
vifolia Engl., and D. pittieri Engl. & К. Krause.

5

in Martiuss Flora Brasiliensis. In

i o
—
=

Araceae
treatment 3 species were included and 16 new
combinations made (these within D. seguine and D.
picta). A year later, in his treatment of Dieffen- Very little work was done with Dieffenbachia af-
bachia in DeCandolle's Monographiae Phaneroga- ter Engler (1915). Gleason (1929) described D. pal-

MODERN WORK

672

Annals of the
Missouri Botanical Garden

Table 3. Treatment of Dieffenbachia species by A.

Engler (19

15).

Species treated by A. Engler (1915) Origin As treated in this manuscript
1. D. aglaonematifolia Engl. Paraguay
2. D. antioquensis Linden & André Colombia
3. D. aurantiaca Engl. Costa Rica D. aurantiaca Engl.
4. D. bowmannii Carr. Colombia & Brazil
5. D. brittonii Engl. Colombia
6. D. cannifolia Engl. Peru
7. D. cordata Engl. Peru
8. D. costata Klotzsch Colombia & Peru
9. D. daguensis Engl. Colombia
10. D. enderi Engl Colombia
11. D. gracilis Huber Peru
12. D. humilis Poepp. Brazil & Peru
13. D. imperialis Linden & André Peru
14. D. latimaculata Linden & André Colombia
15. D. leopoldii Bull iosta Rica
16. D. longispatha Engl. & K. Krause Panama D. longispatha Engl. & К. Krause
7. D. macrophylla Poepp. eru
18. D. obliqua Poe Wi Peru
19. D. oerstedii Schot Central America D. oerstedii Schott
20. D. olbia J. L т n & Rodigas Peru
21. D. parlatorei Linden & André Colombia
D. parlatorei var. marmorea Linden & André Unknown
22. D. parvifolia Engl. Brazil
23. D. picta (Lodd.) Schott Brazil? D. seguine (Jacq.) Schott
D. picta var. angustior Engl. Unknown D. seguine (Jacq.) Schott
D. picta var. angustior subvar. angustifolia Unknown D. seguine (Jacq.) Schott
Engl
D. picta var. angustior subvar. jenmanii Unknown D. seguine (Jacq.) Schott
(Veitch) Engl.
D. picta var. angustior subvar. lancifolia (Lin- Unknown D. seguine (Jacq.) Schott
den & André) Engl.
D. picta var. pud subvar. schuttlesworthi- Unknown D. seguine (Jacq.) Schott
ana (Hort. Bull.) Engl.
D. picta. var. ca (Verschaff. & Unknown D. seguine (Jacq.) Schott
Lem.) Engl.
D. picta var. latior Engl. Unknown D. seguine (Jacq.) Schott
D. picta var. latior subvar. amoena Hort. Bull. Unknown D. seguine (Jacq.) Schott
D. picta var. latior subvar. carderi Hort. Bull. Unknown D. seguine (Jacq.) Schott
D. picta var. latior subvar. gigantea (Ver- Brazil D. seguine (Jacq.) Schott
schaff.) Engl.
D. picta var. latior subvar. magnifica (Linden Venezuela D. seguine (Jacq.) Schott
« Rodigas) Engl.
D. picta var. latior subvar. meleagris (Linden Ecuador D. meleagris L. Linden & Rodigas
« Rodigas) Engl.
D. picta var. memoria (Corsi Salviati) Engl. Unknown D. seguine (Jacq.) Schott
D. picta var. latior subvar. mirabilis (Ver- Unknown D. sequine (Jacq.) Schott
schaff.) Engl.
D. picta var. latior subvar. picturata (Linden Venezuela D. seguine (Jacq.) Schott
& Rodigas) Eng
D. picta var. typica Engl. Unknown D. seguine (Jacq.) Schott
24. D. pittieri Engl. & K. Krause Panama D. pittieri Engl. & К. Krause
25. D. seguine (L.) Schott Martinique D. seguine (Jacq.) Schott
— D. seguine (Jacq.) Schott
D. seguine var. decora (Hort. Vershaff.) Engl. Brazil? D. seguine (Jacq.) Schott
Venezuela D. seguine (Jacq.) Schott

D. seguine var. lineata (K. Koch & Bouché)

ng

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Revision of Dieffenbachia

Continued.

Table 3.

Species treated by A. Engler (1915)

Origin

As treated in this manuscript

D. seguine var. lingulata (Martius) Engl. Suriname & Brazil D. seguine (Jacq.) Schott
D. seguine var. lingulata subvar. irrorata Brazil D. seguine (Jacq.) Schott
Mart.) Engl.
D. seguine var. liturata (Schott) Engl. Unknown D. seguine (Jacq.) Schott
D. seguine var. liturata subvar. wallisii (Lin- Unknown D. seguine (Jacq.) Schott
den) Engl.
D. seguine var. nobilis (Hort. Verschaff.) Engl. Brazil D. seguine (Jacq.) Schott
D. seguine var. robusta (K. Koch) Engl. Unknown D. seguine (Jacq.) Schott
D. seguine var. ventenatiana (Schott) Engl. Suriname D. seguine (Jacq.) Schott
D. seguine var. viridis Engl. Wide = in West D. seguine (Jacq.) Schott
Indies, Central and
South America
26. D. weberbaueri Engl. Peru
27. D. weirii Berkl. Colombia

udicola М. E. Br. ex Gleason from Guayana. and
Jonker and Jonker (1966) described D. elegans A.
M. E. Jonk
were described from Venezuela, D. bolivarana С.
S. Bunting (Bunting, 1963), D. liesneri Croat, and
D. longipistila Croat (Croat & Lambert, 1987). An-
other Venezuelan species, D. duidae (Steyerm.) G.

er & Jonker for Suriname. Three species

S. Bunting, was transferred (Bunting, 1988) from
Spathicarpa duidae Steyerm., described in 1951.
Dieffenbachia has been so confusing that floristic
accounts dealing with Central America have been
of little value. Hemsley (1885) listed only a single
species, D. oerstedit Schott, for his Biologia Cen-
trali-Americana. Engler (1915) reported only five
species for Central America, D. oerstedii. D. au-
rantiaca Engl., D. pittieri, D. longispatha, D.
guine, and D. leopoldii Bull. The first four were
properly circumscribed, largely owing to the fact
that he was dealing with little beyond the type
specimens. Dieffenbachia leopoldii has proven to be
a species known only from Colombia. The only
plants Engler (1915) called D. seguine were from
El Salvador, the type country of D. wendlandii,
which he erroneously synonymized with D. seguine.
Dieffenbachia wendlandii differs from D. seguine in
having unilocular ovaries, and a long-tapered spa-
dix that does not protrude forward at anthesis, as
is the case with D. seguine.
Matuda (1954) reported only

ico, whereas Bunting (1965) reported both D. se-

D. seguine for Mex-

guine and D. oerstedii for Mexico, the latter being
a new report. One of the species that Bunting was
dealing with, which he named as D. seguine, is rec-
ognized herein as D. wendlandii.

These earlier floristic accounts for Central Amer-
ica, in addition to being inaccurate, also grossly
undercounted the number of existing species. This

inaccuracy was in part due to a poor understanding
of the collections that existed at the time, but also
to the fact that most collections of Araceae have
been made in the last 25 years. Panama, for ex-
ample, has shown vast increases in the number of
species collected and identified since the treatment
of Araceae in the Flora of Panama. Some genera
have increased by nearly 544% since 1944 (Croat.
1985). Dieffenbachia now has 26 species recog-
nized for Central America, with 77% of them new
to science since work on the revision began. This
represents a 400% increase from the number re-
ported in Central America by previous workers (En-
gler, 1915; Standley, 1937, 1944; Standley & Stey-
ermark, 1958; Matuda, 1954; Bunting, 1965).
Standley’s treatment of the Araceae of the Lan-
Valley (Standley, 1931) dealt with only 2
species, D. oerstedii, which was at least in part cor-
and D. probably D.

standleyi Croat in the present treatment. However,

cetilla

rectly determined, seguine,
in the case of the latter species he did not mention
the almost fully sheathed petiole that is so distinc-
tive on D. standleyi. Standley also confused D. se-
guine with other species, mentioning that it ranged
to El Salvador (probably D. wendlandii) and to the
West Indies (referring to the real D. seguine).

The treatment of the Araceae in the Flora of
Guatemala (Standley & Steyermark, 1958) is es-
pecially confusing. In this treatment they dealt with
four names, D. oerstedii, D. picta (Lodd.) Schott, a
maculate species that I consider synonymous with
D. seguine and not occurring in Central America.
and D. pittieri, which | consider to be а narrow
endemic in the Canal Zone of Panama. Since they
did not cite specimens, it is difficult to interpret
their treatment, but their description of D. pittieri

with a petiole sheathed almost to the apex and

674

Annals of the
Missouri Botanical Garden

ranging from Guatemala to Honduras may be what
I am currently calling D. standleyi. The plant they
were calling D. oerstedii probably was, at least in
part, the species named. The plant they called D.
seguine was probably D. wendlandii. The mottled
plants they referred to as D. picta may have been
cultivated forms of D. seguine, the mottled forms of
which are popular with horticulturists and have
been known to persist in areas of abandoned dwell-
ings.

The Flora of Costa Rica (Standley, 1937) treat-
ment of Dieffenbachia was somewhat less confused,
probably because it was adapted from Engler
(1911) treatment. Because several of the species
types came from Costa Rica, fewer names were mis-
applied. Here Standley treated D. aurantiaca, an
endemic to southwestern Costa Rica, D. leopoldii
(a Colombian species not believed to be in Central
America and perhaps confused with what I am call-
ing D. killipii in the present treatment), D. pittieri,
and D. seguine. Unfortunately, he cited no speci-
mens nor gave any characters by which to recognize
the species. Certainly, no material currently exists
in Costa Rica of D. pittieri or D. seguine.

In the Flora of Panama, Standley (1944) did cite
specimens for four species. Dieffenbachia pittieri is
endemic to the Isthmus of Panama. Standley (194:
cited the type, Pittier 3766, but he also cited ma-
teria] from El Valle (Alston & Allen 1839) that rep-
resents D. crebripistillata. Dieffenbachia aurantiaca
was even more confused, with only one of the cited
collections, Woodson & Schery 861, being D. au-
rantiaca. Other collections cited assign to three dif-
ferent species, D. isthmia, D. killipú, and D. ton-

A
—

аии, A total of five species were represented
among the 12 collections cited as D. oerstedii, only
one of which actually was that species (Pittier 2836
in western Panama). Other specimens cited under
this name belong to D. isthmia, D. killipii, D. ni-
tidipetiolata, and D. obscurinervia.

COLLECTING HISTORY OF DIEFFENBACHIA

Collecting Araceae has not been particularly
popular, and this would be especially true for Dief-
fenbachia. Many collectors who have been careless
when collecting Dieffenbachia found themselves
badly burned with the often high concentrations of
oxalic acid in the cut parts. Perhaps this has lec
to the generally low numbers of collections of Dief-
fenbachia. A survey of those who collected in Cen-
tral America, based on the extensive TROPICOS
database of collections, shows that aside from my-
self (338 Croat collections for Central America out
of a total of 537 Croat collections in the Neotropics)

relatively few botanists made many collections of
Araceae. Mike
made 68 collections of Dieffenbachia in Central
America, mostly Costa Rica, out of a total of 73
Dieffenbachia collections for that country. Barry
Hammel, a close associate of Grayum and myself,
made 57 collections of Dieffenbachia in Central
America. Paul Standley, one of the most ambitious
collectors in the Neotropics made 54 collections.
Julian Steyermark, another giant in the field of col-
lecting, made 46 collections, but only 13 of these
were in Central America (Guatemala), whereas the
balance were from Venezuela. Al Gentry also col-
lected a lot of Dieffenbachia, 57 in all, but even
fewer were from Central America (only 5 collec-

Grayum, also an aroid specialist,

tions).

The earliest botanist to collect Central American
species of аи was Friedrich Carl Leh-
mann over a century . These were D. killipii
(Lehmann 5311) and р ‘de zii (Lehmann 8876),
the latter as early as 1819. Herman Wendland col-
lected D. wendlandii, in this case before 1858. Oth-
er collectors included Adolfe Tonduz (D. aurantia-
ca) and Henri Pittier, collect
pas (Pittier 2715), D. obscurinervia (Pittier

‚ D. pittieri (Pittier 3766), and D. killipii (Pit-
tier 2600), all collected as early as 1911; Paul Stan-
dley, who was the first to collect D. concinna (Stan-
dley 36739), D. isthmia (Standley 29867), and D.
beechiana (Standley 36840), all in 1924; Paul Allen
initially collected D. crebripistillata (Allen 1839) in
1939; E. P. Killip, D. nitidipetiolata (Killip 35113)
in 1939; and Louis O. Williams, D. horichii (Wil-
liams 28479) in 1965.

Other Central American species were collected
only in the past few decades. Dieffenbachia burgeri
dates to William Burger and Ronald Liesner (Bur-
ger & Liesner 7254) in 1970, and D. davidsei was
not seen until Scott Mori made his collection in
1974 (Mori et al. 4184). Tom Croat encountered
Dieffenbachia fortunensis in 1976 (Croat 37268), D.
galdamesiae in 1979 (Croat 49124), and D. pana-
mensis in 1974 (Croat 27206). Dieffenbachia gra-
yumiana was first noticed by Burger and Matta in
1967 (Burger & Matta 4181), D. fosteri by Robin
Foster in 1993 (Foster е! al. 14649), and D. ham-
in 1978 (Neill & Vincelli

the first to

melii by David Neill i
3484

SUPRAGENERIC CLASSIFICATION OF SUBFAMILY
PHILODENDROIDEAE AND RELATIONSHIPS
OF DIEFFENBACHIA

Engler (1915) placed Dieffenbachia in the sub-
family Philodendroideae Engl. The same position is

Volume 91, Number 4

Croat
Revision of Dieffenbachia

taken by Bogner and Nicolson (1991) in their mod-
ern revision. Grayum (1984, 1990) placed Dieffen-
bachia in its own tribe and does not disagree with
Bogner and Nicolson about its relative placement
or taxonomic status. However, Grayum substantially
modified the Philodendroideae by including the ge-
nus Calla and thus mandated a change in the name
of the subfamily to Calloideae Endl. on the basis
of priority. This group, as defined by Grayum, is
substantially larger than that of Bogner and Nic-
olson’s, with 40 genera arranged in 17 tribes in five
alliances. This contrasts with 18 genera in 7 tribes
according to Bogner and Nicolson. The latter sys-
tem closely mirrors Engler’s Philodendroideae, ex-
cept for the inclusion of new genera and the syn-
onymizing of others since the time of Engler. The
size of Grayum's Philodendroideae resulted from
Aro-

Lasioideae

the inclusion of tribes from the subfamilies
ideae Adans., Pothoideae Engl., and
Engl. (Croat, 1990 1992).

In recent suprageneric classifications by Mayo et
al. (1997, 1998) all the genera with unisexual flow-
ers were grouped together in the subfamily Aro-
ideae and further divided into non-ranked groups.
the perigoniate Aroideae and aperigoniate Aro-
ideae. Dieffenbachia, in the latter group, was placed
in the Dieffenbachia alliance, one of four alliances
(the others called Philodendron, Schismatoglottis,
and Caladium alliances respectively). These alli-
ances comprise 33 genera with an additional 37

‘No alli-

was able

genera а being placed in a group labeled *
ance." The classification by Mayo et al.
to make use of the results of the recently completed
chloroplast DNA studies and anatomical studies of
French and colleagues (1995, 1997). Dieffenbachia,
along with. Bognera, was placed in the tribe Dief-
fenbachieae, a tribe characterized by having the
pistillate flowers completely adnate to the spathe.
In the most recent suprageneric classification of
the family by Keating (2002. 20038) Dieffenbachia
is included in subfamily Philodendroideae, tribe

Spathicarpeae Schott, along with Bognera, Spa-
thantheum Schott, Gorgonidium Schott, Synandros-
Gearum М. E. Br., Spathicarpa Hook.,
& C. A. Mey,

Schott, and Taccarum Brongn. ex Schott. Keating’s

padix Engl.,
Asterostigma | Fisch. Mangonia
revision makes use of a wealth of vegetative ana-
tomical information he has accumulated on the
family. All members of the Spathicarpeae share in
common Туре B collenchyma; vascular bundle type
П (or occasionally types I or Ш); and either lack
laticifers or have non-anastomosing type laticifers.
The Dieffenbachia alliance of Mayo et al. (1997)
is distinguished by having simple laticifers and free
the Dieffenba-

synandria. It contains two tribes,

chieae with two genera (Dieffenbachia and Bog-
nera) and the tribe Spathicarpeae with eight genera,
Mangonia, Taccarum, Asterostigma, Gorgonidium,
Synandrospadix, Gearum, Spathantheum, and
Spathicarpa. Their tribe Spathicarpeae differs from
the tribe Dieffenbachieae in having tuberous stems
and leaves with reticulate higher-order venation.
However, the latter character is also present in
Bognera, one of the two genera in their tribe Dief-
fenbachieae. In the Dieffenbachia alliance Dieffen-
bachieae are distinguished from other tribes by
having anatropous ovules; the primary lateral veins
forming a single marginal vein but also lacking col-
lective veins; and, perhaps most importantly, in
having the pistillate portion of the spadix complete-
ly fused to the spathe. Tribe Dieffenbachieae sensu
Mayo et al. (1997) is distinguished from other tribes
of subfamily Philodendroideae by having stamens
connate into synandria, and in having several free
staminodia associated with the female flowers. Oth-
er useful distinguishing features include a con-
stricted spathe partly adnate with the pistillate spa-
dix, terrestrial caulescent habit, closely parallel
primary and minor veins, and seeds with endo-
sperm.

The Dieffenbachia alliance of Mayo et al. (1997)
has been supported by molecular studies with chlo-
2004).

This study shows close relationships between

roplast trnL-F genes (Barabé; Tam et al.,
Spathicarpeae and Dieffenbachieae with Dieffen-
басма being paired with Spathicarpa on one
branch and with Cercestis Schott, Rhektophyllum N.
E. Br.,
branch of the tree.

Although both Grayum (1984, 1990) and Bogner
and Nicolson (1991) placed Dieffenbachia in its
own tribe, the authors of both systems now agree

and Culcasia P. Beauv. forming another

that. Bognera, another Neotropical genus, is very
close to or within the tribe Dieffenbachieae, sensu
Mayo et al. (1997). Keating (2002, 2003a) simply
subsumed this tribe (or its genera) within his larger
Spathicarpeae, still in essential agreement.

The subfamily Philodendroideae is worldwide in
distribution and, sensu Grayum (pers. comm.), it is
somewhat equally divided between the Old World
and the New World, with 19 genera (17 of them
endemic) and 761 species in the New World and
23 (21 endemic) genera and 354 species in the Old
World. Grayum places the Dieffenbachieae in his
Aglaonema alliance with Zantedeschieae Engl.
Engl.

Zantedeschia Aglaonemateae

re

Spreng.),
(Aglaonema Schott, Aglaodorum Schott), Spathicar-
peae (Mangonia, Asterostigma, Synandrospadix,
Taccarum, Gorgonidium, Gearum, Spathanthemum,
Spathicarpa), and Bognereae S. Mayo & D. Nicol-

Annals of the
Missouri Botanical Garden

son (Bognera). Anubiadeae Engl. (1876) (Anubias
Schott) and Zantedeschieae are restricted to Africa,
while the Spathicarpeae are restricted to southern
South America.

` VEGETATIVE STRUCTURES

—

MORPHOLOGY (

HABIT AND GROWTH PATTERNS

Dieffenbachia is always terrestrial and caules-
cent (Croat, 1988 [1990]. In terms of growth be-
havior and habit, Dieffenbachia is not as variable
as Philodendron, a related genus, but sterile plants
disassociated with notes about habit can be con-
fused with those of Philodendron. Stems of Dieffen-
bachia are erect, at least on the vounger portions.
with older portions of the stem typically becoming
decumbent. This creeping portion of the stem is
sometimes even longer than the erect portion (Fig.
23A). The overall height of any species is usually
determined by the thickness, strength, and rigidity
of the stem. Typically, species such as D. burgeri,
D. hammelii, and most plants of D. oerstedii, with
small-diameter stems, do not get to more than 1 m
tall nor do they usually have stems more than 2.5
em in diameter. Alternatively, the taller species like
D. horichii, D. longispatha, and D. standleyi have
thick stems and reach heights of 2 to 3.5 m. Cul-
tivated plants growing in a pot and unable to be-
come reclined at the base can grow to indefinite
height. A plant of D. standleyi cultivated in the
greenhouse of the Missouri Botanical Garden grew
up the side of a wall from a pot to the height of 8

n.

The portion of the stem that comes in contact
with the ground becomes rooted at the nodes, but
stems are rarely buried. Instead, the stems usually
creep over the surface of the ground. The growth
behavior often leads to vegetative reproduction,
since on some species the creeping portion of the
stem tends to produce active branch buds that form
new growth. Another feature that tends to induce
additional branching is the often fragile stem ex-
which may Бе
Broken
stems invariably produce new branches. These re-
sults often cause Dieffenbachia to grow in large col-

tending laterally over the ground,
broken by being walked on by animals.

onies, especially in open, better illuminated areas
of the understory of a forest, along stream banks or
in open swamps. Examples of colonial growth occur
in D. crebripistillata, D. isthmia, D. killipii, and D.
oerstedii. Some species, such as the taller D. lon-
gispatha (to 3.5 m), are usually less colonial. This
is perhaps because it is a species with a large, stout
stem that is less likely to be broken up by the el-
ements. This species also has a thicker sap that is

more foul-scented and caustic than many other spe-
cies, and may in part account for less breakage by
deterring animals from the plant.

In some cases Dieffenbachia may grow in stand-
ing water. In such cases the stems may be rather
deeply buried in the mud. Some species, such as
D. grayumiana, are frequent in wet habitats, but
most species thrive in well-drained soils. The genus
is seldom found on road embankments, a habitat
that is very common for species of Anthurium and
Philodendron. This is perhaps because the two lat-
ter, principally hemi-epiphytic genera сап more
easily become established on the excessively well-
drained and poor clay soils of typical road em-
bankments in the Neotropics.

Development in Dieffenbachia is never hetero-
blastic. Instead, changes in internode size and leaf
size progress without any marked changes in blade
shape. However, leaf blades of Dieffenbachia that
ultimately become cordate at the base are at first
simple and acute to obtuse at the base.

STEMS

Internodes are typically about as long as broad

or even shorter than broad. Sometimes, as in the

case of D. galdamesiae, petioles are affixed to the

stem at an oblique angle and the internodes are not
of equal width across the diameter of the stem. In-
stead, one side is as much as 1 em wider than the
other. Most commonly, internodes are glossy to se-
miglossy and smooth, though they may be minutely
roughened, appearing with a somewhat weak vel-
vety sheen, as in the case of D. oerstedii. Though
for most species the internodes remain moderately
glossy even in age, when fresh, the internodes may
change promptly. In D. the stem,
though initially semiglossy, promptly becomes

obscurinervia,

etched in a deep, areolate pattern to such an extent
that the stem becomes matte and is conspicuously
scurfy.

Cataphylls are never present on Dieffenbachia.
Instead, the new growth on stems of Dieffenbachia
is protected by the sheathing petiole of the preced-
ing leaf.

Stem color varies considerably between species
and even within populations of the same species.
Species such as D. longispatha, which typically
possess stems that are solid green, can sometimes
be variegated with paler colors. Typically, stem col-
or variegation is in the form of streaks rather than
mottling. The stem may be relatively dark green
with even darker streaks, in which case the mot-
tling would not be too apparent, or, as is more fre-

quently the case, it may be streaked with pale

Volume 91, Number 4
2004

Croat 677

Revision of Dieffenbachia

green or yellow-green. Dried stems are often highly
diagnostic for key characters such as the degree to
which they are contorted, usually

cracked, or the color that they dry.

LEAVES

eaves may be clustered near the apex of the
stem such as in Dieffenbachia panamensis or some-
times they are rather well scattered along the stem
as in D. grayumiana.

Dieffenbachia petioles are on average shorter
than the blades, ranging from 0.23 to 1.08 as long
as blades, and averaging 0.65 times as long as
blades. Typically, the blades average about 1.5
times longer than the petioles. The petioles are typ-
ically sheathed for a significant portion of their
length. The extent and nature of the leaf sheath
constitutes one of the most important species-level
characters. The sheath margins are virtually always
persistent, but the degree to which the sheath is
open, i.e., erect-spreading (Fig. 24D), erect, or in-
The
petiole sheaths of D. wendlandii are typically in-

rolled. remains an important characteristic.
rolled at the apex, whereas the sheath of D. oerste-
dii is erect. The petiole sheath is typically unequal
at the apex with one side more acute than the other.
Some species (D. davidsei, D. seguine) have the pet-
iole sheath free-ending (Figs. 8D, 23D).

Petiole cross-sectional shape is given only for the
free portion of the petiole (when present). While
sometimes variable within the species, it often con-
stitutes an important taxonomic difference between
species. Petioles are most commonly subterete with
the adaxial surface frequently somewhat flattened
(as in D. longispatha, Fig. 16C) or sulcate (D. be-
achiana, Fig. 3D). When sulcate the petioles may
be obtusely alia or sharply sulcate, as is usually
the case in D. oerstedii (Fig. 20D). Though rare, the
petiole cross-sectional shape may be triangular, as
in D. aurantiaca where, in addition to being flat-
tened adaxially, the lateral margins are bluntly
winged and spreading (Fig. 2C, D). In D. pana-
mensis the free portion of the petiole is also winged:
the wing itself is usually thin, spreading, and mark-
edly undulate. The free portion of the petiole may
also have a prominently winged margin with the
wing itself usually thin and undulating as in D

a and D. standleyi (Fig. 24).
Dieffenbachia has leaf blades usually consider-
ably longer than the petioles, ranging from 0.9 to
4.3 times longer than the petioles. Blades are typ-
ically conspicuously longer than wide, ranging from
1.1 to 4.3 times longer than wide. The blades are
similar to those of many species of Philodendron.

ridged or

fortunensis (Fig. 9C).

and sterile specimens for which habit is not men-
tioned are often difficult to separate from Philoden-
dron. Most leaf blades are ovate to oblong-ovate,
elliptic, oblanceolate or obovate, and are usually
acuminate at the apex and acute to obtuse or round-
ed at the base (rarely subcordate at base as in D.
As is true of Philoden-
dron, Dieffenbachia vernation is always supervolute
(Cullen, 1978).

Venation patterns are similar to those in Philo-

wendlandii and D. isthmia).

dendron (cf. Croat, 1997). The midrib is especially
variable and diagnostic, especially on the adaxial
surface, being usually prominently raised and vary-
img from angular to broadly convex. The shape of
the midrib is often taxonomically significant. In D.
killipii the upper midrib is raised with square mar-
gins (Fig. 15B, С). In other cases the midrib may
be broadly convex as in D. panamensis (Fig. 21D)
or flat to sulcate as in D. standleyi. The midrib color
is also important, since the midrib may be con-
spicuously paler than the lamina as sometimes in
D. oerstedii (Fig. 20) or concolorous as in D. gal-
damesiae (Fig. LOB). In D. obscurinervia the midrib
may be conspicuously speckled as is the petiole
(Fig. 19C).

Primary lateral veins are usually well spaced
with many, much finer minor veins between each
pair of primary lateral veins. In all cases, the pri-
mary lateral veins extend to the margin and do not
form a collective vein that extends all the way to
the apex. Instead the primary lateral veins typically
course along the margin of the blade, where they
may form a weak collective vein that joins several
primary lateral veins (especially near the middle of
the blade) that eventually merge with the margin
before reaching the apex. Primary lateral veins are
usually somewhat sunken to weakly quilted-sunken
above and raised on the lower surface (sometimes
thicker than broad and sometimes weakly pleated-
raised). Blades of D. davidset may be rather con-
spicuously quilted-sunken (Fig. 8B). Leaf blades
typically are glabrous, but the major veins may
rarely be puberulent, as in D. beachiana, to gran-
ular-puberulent or conspicuously granular, as in D.
y ). Minor veins may arise only
from the midrib, as appears to be the case in D.
longispatha and D. nitidipetiolata, or they may
arise from both the midrib and the primary lateral
veins. The latter situation appears to be the most
common in Dieffenbachia.
MORPHOLOGY OF FLOWERING STRUCTURES
INFLORESCENCES

Dieffenbachia inflorescences are far less diag-

nostic than those of Philodendron, since nearly all

678

Annals of the
Missouri Botanical Garden

are solid green on both surfaces. There are consid-
erable differences in the number of inflorescences
per axil, ranging from solitary on a number of spe-
cies at least part of the time or up to eight per axil
as with D. concinna. In any population the number
of inflorescences per axil may vary. Studies made
with D. oerstedii in Costa Rica (Valerio, 1984
showed that this species produced primarily one or

—

two inflorescences per axil.

SPATHE

=)

Each spathe cluster of inflorescences it
Dieffenbachia is subtended by
bracteoles, each of which are unribbed.
teoles are typically about as long as the peduncles,
but can sometimes be shorter or longer. They are

linear-lanceolate
The brac-

somewhat marcescent.

Spathes of Dieffenbachia are uniformly green,
though the inner surface tends to be somewhat pal-
er than the outer surface and frequently much
glossier. The outer spathe surface is typically se-
miglossy to weakly glossy. Sometimes the inner sur-
face of the spathe is somewhat whitish on the inside
near the tip.

The spathe of most Dieffenbachia 1s only weakly
constricted above the spathe tube (Figs. 7A, 16D,
20F, 22E, 23E, 24F, 25F). When the entire spathe
is fully flattened, the tube portion is considerably
wider (Figs. 2B, 15H, 22F, 23F) and the spathe is
gradually tapered from the lower М to the usually
acuminate apex (Fig. 23F). Sometimes there is a
weak central constriction. The point of maximum
constriction corresponds to the sterile section of the
spadix between the fertile staminate flowers and the
pistillate flowers

At anthesis the spathe of Dieffenbachia is open
to about the middle (Figs. 5B, 7A, 13E, 16D). o
somewhat below the middle, but does not open as
widely as that of Philodendron. At anthesis the
spathe blade is wider than the tube. Typically only
the staminate portion of the spadix is visible at an-
thesis but sometimes, as in D. crebripistillata, a por-
tion of the pistillate spadix is also exposed. Closure
of the spathe after anthesis is sometimes not com-
plete, with the margins of the spathe meeting irreg-
ularly. At anthesis the blade of the spathe is usually
arched somewhat forward, hooding the spadix
slightly. For some species, such as D. crebripistil-
lata, the spathe may be recurled at anthesis (Fig.

aje

SPADIX

Flowers of Dieffenbachia are unisexual and na-

ked, dispersed on the spadix in the typical manner

with the staminate flowers at the apex and the pis-
tillate flowers at the base. The spadix of Dieffen-
bachia is usually shorter than the spathe by 1—
cm (Fig. 2B). The spadix is contained within the
spathe, and is more or less straight or weakly
curved (Fig. 8F) at anthesis, rather than being
prominently protruded forward. Some species have

the spadix protruded forward at anthesis, such as
D. burgeri (Fig. 4C), D. crebripistillata (Fig. 7C), D.
horichii (Fig. 13E), D. wendlandii (Fig. 26C), and
D. seguine (Fig. 23E). The last species, which rang-
es throughout the West Indies, has a spadix that
notably protrudes and is cylindrical, rather than ta-
remaining Central

—

pered to the apex as in tl
American species (Fi ig. P 3F). Dieffenbachia seguine
also has a spadix (Fig. 23) that is caught in the
protruded position when the spathe re-closes. In
contrast to D. seguine, all of the Central American
species have spathes that close d with the
spadix withdrawing inside of the spat

Like other members of the Philodendroideae, the
spadix in Dieffenbachia is divided up into a fertile
staminate section at the apex, a sterile section lying
beneath the fertile staminate portion, and the pis-
tillate portion (Figs. 2B, 7, 18, 25). The lowermost
section, as with all Araceae with unisexual flowers,
is the pistillate section. Typically the pistillate por-
tion and the staminate portion are of roughly equal
lengths, but the length of the sterile segment (when
apparent) is highly variable both in terms of length
and the degree to which staminodia and pistillodes
are dispersed on it (Figs. 2B, 4C, 5D, 7, 15H, 18D,
23K, 25G). In most cases the pistillate region is
d longer than the staminate.

e fertile staminate portion is somewhat cylin-
droid t to spindle-shaped, broadest in the middle and
tapered toward both ends, being bluntly
The fertile male flowers are

weakly
rounded at the apex.
compacted and sub-rounded or with angular mar-
gins (Figs. 2E, 5G). As the spadix approaches an-
thesis the synandria loosen and the anthers become
visible between the synandria. Toward the base of
the staminate portion of the spadix, the flowers are
somewhat more irregular in size and shape, but do
not become radically different as in the case of
Philodendron and Xanthosoma, where the lower-
most male flowers are sterile and swollen. In con-
trast, Dieffenbachia relies entirely on club-shaped
staminodia surrounding the pistils (Figs. 5E, ТАС).
The lowermost staminate flowers are smaller or very
irregular in shape, sometimes showing signs of two
or more flowers fused together. Sometimes the up-
permost pistils are reduced, apparently sterile, and
surrounded by sterile male flowers (Fig. 15H). Ap-
parently the lowermost staminate flowers are also

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

more attractive to beetle pollinators, since only the
lowermost flowers are eaten (Fig.

ANDROECIUM

Staminate flowers consist of 4 stamens united
into a 4- or 5-suleate truncate synandrium (Figs.
2E, 5G, 236. 26E). The apex of the synandrium

often has a minute slit or an equidistant series of

З minute slits connected at the center. Upon drying
the apex of the synandrium may become wrinkled
along the margin and may also have a concave sur-
face. The anthers are contiguous or nearly so, af-
fixed near the upper edge of the synandrium. The
thecae are obovoid to cylindroid, opening by apical
slits just below the upper edge of the synandrium.
The pollen is dispersed in slender, subterete fila-
ments and typically projects up to 1 em above the
surface of the synandrium. When the stamens are
at anthesis, the shedding pollen can completely fill
the now closing spathe (Fig. 5

POLLEN

Pollen of Dieffenbachia is released in monads
that are inaperturate, subisopolar to virtually polar.
boat- shaped-elliptic to oblong, or nearly spherical.

ey are bilaterally symmetrical or radiosymmetric
(Grayum. 1992).

Dieffenbachia pollen is moderately large for Ar-
aceae, ranging from 54 to 99 jum (as in D. verstedii)
and averaging 79 wm. Exine sculpturing is psilate
to obscurely verruculate (as in D. oerstedii) and/or
sparingly punctate-foveate to densely foveate with
scattered compound foveolae (as in D. pittieri and
Grayum (1992) pointed out that the
compound foveolae found on the pollen of D. pittieri
and D. seguine resemble those of Chlorospatha
croatiana Grayum.

—

D. seguine).

STERILE SPADIX SECTION

Dieffenbachia typically has a nearly barren sec-
tion of the spadix lying between the fertile stami-
nate portion at the apex and the pistillate portion
at the base (Figs. 5D, 23F). This section occurs in
the area where the spadix first becomes free from
the spathe. Only rarely is the transition between
the fertile staminate and the sterile portion of the
spadix clearly defined with the fertile flowers
abruptly ending on a clear flowerless sterile portion.
Instead, there is usually an assortment of sterile
male flowers toward the apex of the sterile segment
(Fig. 7E). Less frequently there are pistillodes in
the lower half of the sterile segment. In D. beachi-
ana and D. killipii (Fig. 15H) the sterile section is

apparently absent, with the fertile staminate and
fertile pistillate portions essentially contiguous. The
length of the sterile portion of the spadix is here
defined as that portion which lies between the low-
ermost functional androecium and the uppermost
functional pistil regardless of the presence of pis-
tillodes and staminodes along its length. However.
the sterile portion of the spadix is usually quite
obvious since a significant proportion of the sterile
section is devoid of flowers. The axis of the sterile
portion is typically convex as if the terete axis of
the spadix (now fused) was half sunken into the
leafy tissue of the spathe.
PISTILLATE SPADIX

The pistillate portion of the spadix is fused
throughout its entire length to the spathe. What ap-
pears to be a stipe is readily apparent at the base.
The pistillate flowers rarely extend very close to the
base of the spathe (Fig. 4C). After the presence or
absence of a sterile segment in the spadix, the
number and disposition of the pistils is perhaps the
most important taxonomic character in the inflores-
cence. Unlike many genera in the Philodendroideae
that have the pistillate flowers closely aggregated
on the spadix, the pistillate flowers of Dieffenbachia
are moderately dispersed on the spadix. The degree
of dispersal on the spadix is in itself different ner
species to species. There are generally only 2 or
pistils across the width of the spadix axis dea
less of whether they are lined up or not). Rarely,
as in the case of D. killipii, there up to 6 pistils
visible across the width of the spadix. At the op-
posite extreme, D. longispatha sometimes has a sol-
itary row of pistils across the spadix axis. The ar-
rangement of the pistils is generally quite irregular,

acking any obvious equidistant spacing or align-
ment in rows, but sometimes a series of pistils
might be arranged in a loose row (as in D. Killipii)
or even in a broad arc across the width of the spa-
dix.

Pistils are 2- or 3-carpellate, sometimes l-car-
pellate, sessile, depressed-globose to depressed-
ovoid, pale green, semiglossy, and smooth or 2- or
3-lobate.
like layer that covers the entire apex of the pistil.

The stigma is a 2- or 3-lobate cushion-
The stigmatic papillae are orange or yellow. The
papillae are close, dense, and moderately short,
similar to those of Philodendron, but appear less
interspersed with the gelatinous matrix that is so
common on the stigmas of that genus. The stylar
region is inconspicuous. With the stigma removed,
the surface is truncate or broadly sulcate with a

solitary medial or near-medial pore. Ovules are

680

Annals of the
Missouri Botanical Garden

anatropous, one per locule. Each pistil is surround-

by 4 or 5 claviform, fleshy, white staminodia.
The staminodia may be fused somewhat at the base,
often forming a cupuliform structure around. the
base of the pistil. Individual staminodia are sub-
cylindrical, commonly somewhat flattened toward
the base and usually enlarged, sometimes almost
subglobular at the apex. Staminodia typically are
erect-spreading or erect, vary considerably in
length, but are almost invariably longer than the
pistils, usually 2-5 mm long, and held well above

the. pistils.

MORPHOLOGY OF FRUITING STRUCTURES

INFRUCLIESICERINLIE AND ЕКІ IT

While the inflorescences are always first. erect,
they quickly become reflexed after anthesis. This

is probably important to successful development of

the infructescence as it prevents the spathe from
filling with rainwater and thus possible decay.

Fruits develop within the re-closed spathe, which
often turns yellow, pale to bright orange, or red as
fruits begin to mature. The spathe enlarges some-
what during the course of maturation, and finally
begins to reflex along the middle, especially the
portion that is fused to the spadix. In the process
most of the margins of the spathe slough off, leaving
just the fruiting spadix. The spadix remains arched
backward with the bright red to orange-red berries
held somewhat apart by the recurving process and
displayed against the generally pale remains of the
spathe (Figs. 1D, 4D).

Although fruit develops with self pollination,
fruit and seed size are greater when the plants are
1986). Since Dieffenbachia
flowers are naked, all protection of the flowers must

out-crossed (Young,

be provided by the spathe. In the manner of many
other genera in the Philodendroideae, the spathe
re-closes over the female flowers after pollination.
In most cases, protection of the developing fruits
after pollination is provided by the thickness of the
spathe, as is true of other aroid genera such as
Philodendron, but in Dieffenbachia protection is
also provided by toxins in the sap, which may burn
the mouth of any animal eating it. However, the
pericarp and mesocarp of the berry appear to have
no injurious effects when eaten and apparently lack
the same toxic effects found elsewhere.

Generally, most pistils of an inflorescence are
pollinated and develop into fruits, but the number
produced per plant is variable. Studies in Costa
Rica on D. oerstedii (Valerio, 1984) showed that the
fruits varied from 13 to 43 with an average of 26
per plant. Valerio also reported that some berries

were sterile, varying from 1 to 17 per infructesc-
ence

Germination of seeds is usually prompt if the
1984) found that

naked seeds of cleaned berries of D. oerstedii began

—

mesocarp is first removed. Valerio

to germinate within four days in a germination
chamber. The percentage of seeds germinating
ranged from 77.3% to 100% for different infruc-

escences (averaging 91.7%). However, berries left
Sing

—

intact usually did not germinate, but remainded vi-
able for up to 90 days.

Valerio (1984) also reported that although 82%
of the 729 berries studied were green, the remain-
der were red or yellowish. All seeds produced only
albino plants. Germination rates for both the green
seeds and the abnormal seeds were the same, but
the albino plants perished. His studies with seed
germination of D. oerstedii, as well as observations
of other plants in the field led him to conclude that
plants of this species required between five and six
years to reach reproductive age.

Fruit maturation is normally a slow process in
Dieffenbachia, requiring up to nine months in the
case of D. nitidipetiolata (Young, 1986) (reported
(1984) reported that
fruit maturation in D. oerstedii was approximately

as D. longispatha). Valerio

one year. Valerio (1984) suggested that the seeds
of Dieffenbachia are bird-dispersed because the
seeds will not germinate unless the fruit mesocarp
is first removed. At maturity the mesocarp of Dief-

fenbachia berries is pasty and somewhat sweet. The

fruits would appear to be most suitable to bird dis-
persal, being colorful and having only a thin layer
of edible portion available. The seeds are soft and
could easily be destroyed by chewing, so effective
animal dispersers are probably just removing the
pericarp and thin mesocarp. Fruits of Dieffenbachia
have been observed being eaten by white-faced
monkeys, Cebus capucinus (J. Oppenheimer, pers.
comm.), but it is not known whether they are the
primary dispersal agents, since cebus monkeys are
known to be generalists in their eating behavior (J.
Oppenheimer, pers. comm.).

FLOWERING BEHAVIOR AND POLLINATION

Dieffenbachia populations tend to be aggregated,
perhaps due as much to the vegetative reproduction
of the stems as by local germination of seeds.
single clone may have many stems, but relatively
few stems flower in a given year, and the number
of inflorescences open on a given day is few (Young,
1988b). Inflorescences borne on a single stem gen-
erally do not anthesally overlap, thus there is little
potential for geitonogamy (Young, 1990). For D. ni-

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2004

Croat 681

Revision of Dieffenbachia

tidipetiolata (reported as D. longispatha in Young,
1988b) a reproductive stem may have two to seven
inflorescences during a single growing season, ma-
turing at intervals of 3 to 12 days (Young, 1986).
For D. oerstedii there may be between one and four
inflorescences per axil. Valerio (1984) reported that
plants which produced a solitary inflorescence (34
of the 83 plants studied produced inflorescences)
did not develop fruit. Valerio was unable to ascer-
tain whether this was due to a lack of pollinators
or age of the plants.

The pollination biology of Dieffenbachia has
been studied (Croat, 1978, 1983b; Valerio. 1984:
Young, 1986, 1988a, 1990). It has long been known
to aroid workers that Dieffenbachia and several oth-
er aroid genera, e.g.. Philodendron, some Syngon-
ium, and Xanthosoma, are visited regularly by large
scarab beetles (Coleoptera). Young (1986. 1990)
found that D. nitidipetiolata (reported as D. longis-
patha) is pollinated mostly by beetles of the genus
Cyclocephala (Scarabaeideae, Dynastineae) or more
infrequently by the genus Erioscelis, also a dynas-
tine scarab. Other visitors, including Diptera. He-
miptera, Dermaptera, Thysanoptera, and nitidulid
Nitudulidae).
carry pollen and were deemed by Young not to be
pollinators (Young, 1990).

Other monoecious aroid genera, such as Philo-

beetles (Coleoptera, proved not t

dendron and Xanthosoma, are known to be beetle
pollinated and provide food by means of oil-rich
sterile male flowers. In Dieffenbachia the food re-
ward consists of the protein-rich club-shaped sta-
minodia surrounding each female flower (Young.
1986, 1990), but the beetles have also been seen
feeding on the lowermost portion of the fertile sta-
minate portion of the spadix. An indication that the
staminodial food source is important to the beetles
and preferred over other floral parts. is that the
beetles will leave an inflorescence.

1e. production of scents during flowering is fa-
cilitated by the thermogenic behavior of the spadix.
which may increase as much as 4°C during anthesis
(Young, 1990). Scent production coincides with the
flight activity of the scarab beetle pollinators
(Schatz, 1990). Active movement of pollinators is
usually at dusk, seemingly in direct paths to an
open inflorescence. Beetles arrive at the inflores-
cence by first landing on the spadix (Young, 1990),
then entering the lower tube portion of the spathe
where the pistillate portion of the spathe is at an-
thesis. Beetles typically remain in the inflorescence
for 24 hr. after their arrival. While in the spathe
the beetles mate and eat the nutritious staminodia
(Young, 1986) surrounding the pistils. Beetles de-
part the following day as the inflorescence begins

to close and the staminate flowers are emitting pol-
len in long filaments (Fig. SF). In order to leave the
inflorescence the beetle must literally wade through
pollen, ensuring that it will be covered with pollen
before flying away to the next receptive inflores-
cence.

While some Dieffenbachia species, perhaps
most, have spathes that remain open only 24 hr.
(based on my observations in the field), the polli-
nation event for D. ni
Young as D.

(Young. 1990). Inflorescences of this species open

nitidipetiolata (reported. by
longispatha) involves three days

in the evening of the first day, but the spadix is not
initially. receptive. On the evening of the second
day the stigmas become receptive (about 17:30)
and the spadix temperature increases to 4°C above
1990).
time that beetle pollinators arrive, and they enter

ambient. temperature (Young, It is at this
the spathe where they generally persist for another
full day. departing on the evening of the third day.
Young (1990) found that for most days there were
fewer than four inflorescences open and in female
phase at any one time in an area of 700.000 m. In
her studies at La Selva in Costa Rica she found
that beetles flew between 1 and 680 m (averaging
83 m) between consecutive visits to D. nitidipetiol-
ata. (reported as D. longispatha).

Beetle pollination of Dieffenbachia is not spe-
cies-specific. Nine different scarab beetle species
of Cyclocephala as well as Erioscelis columbica En-
drodi were found to pollinate D. nitidipetiolata (re-
ported by bos. as D. longispatha) at the La Selva
1986). Still. Dief-

Reserve in Costa Rica (Young,

fenbachia species produce different scents and dif-

ferentially attract particular beetle species (G.
Schatz, pers. comm.).

Because of the loose relationship between the
pollinators and any one species of Dieffenbachia,
hybridization does occasionally occur (Young, pers.
comm.). It is known that seeds from hybrid plants

do germinate and produce viable FI plants. It has

not yet been determined if this Fl generation is
capable of reproducing sexually. Still. this phenom-
enon of hybridization might explain the many dif-
ferent, seemingly related, but distinct. populations
of D. nitidipetiolata that occur in some regions,
such as the Río Guanche region of Colón Province
in Panama. Since asexual reproduction is so prev-
alent in Dieffenbachia, occasional hybridization fol-
lowed by vegetative reproduction might explain
these patterns of variation.

PHENOLOGY

Some species of Dieffenbachia are in flower all
year-round. In general, more flowering takes place

Annals of the
Missouri Botanical Garden

during the rainy season even if the species flowers
at other times of the year as well. This may be tied
to the fact that the beetles pollinating Dieffenbachia
are more frequent during wet periods. Although D.
beachiana and D. burgeri flower primarily in the
dry season in Costa Rica and Panama, they occur
in wetter habitats where beetle pollinators are re-
liably available.

CYTOLOGY

Dieffenbachia has chromosome counts of 2n =
34 and 68 (Petersen, 1989). Grayum argued that
Dieffenbachia is closely related to Philodendron
(Grayum, 1984). Petersen (1989) argued that Phil-
odendron would not be considered so closely relat-
ed if its chromosome base number were not 17 as
assumed by Grayum. She also argued that the dif-
ferences in the “size and constitution of the chro-
mosomes (small metacentrics of Philodendron versus
medium to large submetacentrics to subtelocentrics
of Dieffenbachia) also indicate that no close relation-
ship exists between the two genera” (Petersen, 1989:
128). Petersen considered the chromosome basic
number in Philodendron to be x = 18 based on the
fact that all members of Philodendron subg. Me-
conostigma (Schott) Engl. have 2n = 18 and sub-
genus Philodendron Schott also has 2n = 18 1
part. Grayum (1984) suggested that Dieffenbachia
was close to the tribe Spathicarpeae (subfam. Aro-
ideae). Petersen (1989) considered this a reason-
able suggestion since they share the same basic
number of x = 17

=

17 and large chromosomes also with
the centromere frequently located distally on the
chromatids. Petersen (1989) believed that the Agla-
onemateae may be the closest relatives of Dieffen-
bachieae based on the similarity in the constitution
and size of the chromosomes, despite the fact that
the former has a different chromosome base number
(x = 20). Chromosome counts for Bognera recon-
dita (Madison) Mayo & Nicolson, the only other
member of Dieffenbachieae, are also 2n — 34. Bog-
nera, a monotypic genus, also shares a karyotype
of medium-sized

—

metacentric to sub-telocentric
chromosomes with Dieffenbachia (Petersen, 1989)

GEOGRAPHICAL DISTRIBUTION AND ENDEMISM

The genus Dieffenbachia has approximately 135
species, most of them in South America. It ranges
from Mexico, throughout Central America, and to
the West Indies, Trinidad, and most of South Amer-
ica as far south as Argentina, Paraguay, and Boliv-

. Distribution of species is unequal, with 1
centers of diversity

—

including Colombia with :

species, Ecuador (34), Peru (30), Brazil (27). з

ama (20), and Costa Rica (13), principally at lower
to middle elevations in the Andes. The genus is
also widespread in the Amazon basin as is evi-
denced by the large number of species at low ele-
vations in Brazil with a total of 27 species. Only 8
species occur in the Guianas region in eastern
South America and the Territorio Amapá of north-
eastern Brazil. The genus is exceptionally abundant
in the western Amazon basin in the foothills of the
eastern Andes, with 57 species. The wetter forests
at middle elevations in the foothills of the Andes
are particularly rich. For example, there are 5 spe-
in the vicinity of the Jatán Sacha Reserve
Pu the Upper Río Napo near Misahuallí in Ec-
uador.
s is true for many other genera of Araceae
(Croat, 1992, 1983a, 1986a, 1986b), the north-
western part of South America, especially on the
Pacific slope of Colombia and adjacent Ecuador, is
rich in species of Dieffenbachia. About 14 species
occur on the eastern slopes of the Andes in Ecua-
dor and about 15 species are known from the Pa-
cific slope in Colombia. Relatively few species oc-
cur in South with only
Dieffenbachia aglaonematifolia Engl. occurring in
southern Brazil, Paraguay (Croat & Mount, 1988),
and Argentina. Collections of only 7 species, mostly
new species, have been seen for Bolivia. North-
central South America is also not particularly rich
in species. Only 2 species occur in the Cordillera
de Mérida in Venezuela, and only 1 of these occurs
in the Cordillera de la Costa (Bunting, 1979; Croat
& Lambert, 1987).

A preliminary key and preliminary descriptions
have been produced for South American Dieffen-
bachia species, but many species remain poorly
known. Thus the figures given for South America
remain tentative

southern America,

Central American species constitute a group rel-
atively isolated from South America, and only seven
species range into South America, especially along
the Pacific slope and in the Magdalena River Valley
in Antioquia Department. The majority of Dieffen-
bachia in Central America occur from Nicaragua to
Panama, and most are relatively widespread in this
region. The most widespread species of Dieffen-
bachia, D. oerstedii, ranges from southern Mexico
to western Panama (Fig. 29). Dieffenbachia wen-
dlandii ranges from Mexico to Costa Rica (Fig. 28)
and both D. nitidipetiolata and D. tonduzú range
from southeastern Nicaragua to Ecuador (Figs. 30
& 29, respectively). In the latter country, D. niti-
dipetiolata crosses the Andes into the Amazon
drainage in Napo. Remaining Dieffenbachia are all
narrowly isolated. Nine species are shared between

Volume 91, Number 4
2004

Croat 683
Revision of Dieffenbachia

Costa Rica and Panama, but even these are not
widespread in the two countries. Those shared are
D. aurantiaca, D. beachiana, D. davidsei, D. gra-
yumiana, D. killipii, D. nitidipetiolata, D. oerstedii,
D. tonduzii, and D. wendlandii. Dieffenbachia au-
rantiaca occurs only in southwestern Costa Rica in
the vicinity of the Osa Peninsula and in adjacent
Panama in the Burica Peninsula area (Fig. 27).
Both Dieffenbachia р and D. grayumiana
range from northern Costa Rica to western Panama
(Bocas del Toro) (Figs. 2 21), while D. davidsei
ranges from northwestern Costa Rica to central
Panama (San Blas) and Colombia (Fig. 27).

A total of 11 species (42% of the total) of Dief-
fenbachia are endemic to either Costa Rica or Pan-
ama. Endemism is particularly high in Panama
where 8 of the 26 species (31%) are endemic. In
Panama endemic species are D. copensis, D. cre-
bripistillata, D. fosteri, D. fortunensis, D. galdame-
siae, D. lutheri, D. panamensis, and D. pittieri (Figs.
27—30). In Costa Rica 3 of 26 species (12%) are
endemic. Costa Rican endemics are D. burgeri, D.
hammelii, and D. horichii (Fig. 27). Neither Mexico

nor

iddle America have endemic species.
Dieffenbachia isthmia (Fig. 28), D. longispatha
(Fig. 29).
across the Isthmus of Panama from Veraguas Prov-
ince to northern Colombia. Dieffenbachia aurantia-
ca, D. beachiana, and D. grayumiana (Figs. 27, 28)
are the only species occurring in both Costa Rica
and Panama. Some species are further isolated.

and D. obscurinervia (Fig. 29) range

Dieffenbachia aurantiaca and D. burgeri are re-
stricted to the region of the Osa Peninsula in south-
western Costa Rica (or in the case of D. aurantiaca
in Panama on the adjacent Burica Peninsula; Fig.
27) and D. horichii is restricted to a relatively small
area on the Pacific slope of Costa Rica (Fig. 27).
Several other species are also narrowly restricted

known only from the type specimen. Dieffen-
bachia fosteri is restricted to northeastern Panama
(Fig. 27). Dieffenbachia fortunensis is restricted to
the northern Chiriquí Province (Fig. 28). Dieffen-
bachia copensis is found only in the Coclé Province
of Panama (Fig. 27), and D. galdamesiae in a small
area south of the Panama Canal (Fig. 28).

Further collecting in Colombia, especially along
the western slope of the Andes, may change the
distribution of Dieffenbachia, but the current pat-
terns most likely reflect the realities of life zone
ecology and geologic history of the area rather than
under-collecting. Since relatively few species of Ar-
aceae are known to occur at lower elevations on
both the eastern and western side of the Andes, it
can be presumed that the evolution of the respec-
tive Amazonian and Pacific coastal floras occurred

independently after the Andes began to arise to-
ward the end of the Cretaceous (Raven & Axelrod,
1974). The fact that there are no truly wide-ranging
those ranging from Mexico to Brazil,
attests to this isolation. The high rates of endemism

species, i. E.,

in Costa Rica and Panama as well as Mexico per—
haps reflects the isolation of these areas during pe-
riods when the oceans were at much higher levels
than they are today, and when the area that is now
central Panama and Costa Rica was subsequently
disconnected from South America. At the close of
the Tertiary period, 18,000 years ago. the sea level
was about 100 m higher than today (Holmes, 1969).
Much earlier the land mass of what is now Central
America began to emerge as a series of islands dur-
ing the Oligocene epoch with further uplifting dur-
ing the Middle Miocene. It was not until the Upper
Miocene and Pliocene epochs that the final portions
of the isthmus of Panama emerged above sea level
(Torre, 1965), and the final connection of Central
and South America was about 5.7 million years ago.
To put these geological events in relation to the
modern aroid flora, it should be noted that even
during this era precursors to the extant flora prob-
ably already existed. The angiosperm floras of the
Oligocene were believed to have consisted almost
entirely of extant genera and with existing species
among Oligocene and Pliocene floras (Takhtajan.
1969)

Equally important as geology to the isolation of
the Central American aroid flora are ecological fac-
tors for Central American species of Dieffenbachia.
Much of eastern Panama consists of broad expanses
of Tropical moist forest (T-mf) with other, generally
smaller areas of Premontane wet (P-wf) and Tropical
wet forest (T-mf) (Holdridge, 1967). In contrast to
Panama, much of the Chocó area of northwestern
Colombia consists of much wetter pluvial forest
with annual precipitation exceeding 11.700 mm
(Gentry, 1982). This broad band of pluvial forest
with its own suite of unique endemic species no
doubt acts as a dispersal barrier for species from
regions with less rainfall. It may account for those
Panamanian and Costa Rican species that skip the
wettest areas of northwestern South America but re-
occur in the relatively drier areas of mesic western
Ecuador.

Middle America has low species diversity with
Guatemala having only two species and Honduras
three. Only Nicaragua, with six species, four of
them restricted to the southeastern corner near Cos-
ta Rica, is moderately rich in species. All except
D. standleyi and D. wendlandii appear to range into
the country from Costa Rica. The low species di-
versity and very low aroid endemism in Dieffen-

Annals of the
Missouri Botanical Garden

bachia in Middle America is perhaps explained by
its historic remoteness from existing large land
masses to the north and to the south. The distri-
bution of modern aroid species suggests that the
northwestern part of Middle America may have
been isolated from Costa Rica in the area of the
San Juan Depression (Nicaragua). Many of the spe-
cies that occur in Costa Rica or Panama enter into
Nicaragua in only a small area in the southeastern
part of the country. Though the existing flora of
Guatemala does not reflect isolation from Mexico to
the same degree, it is possible that the more ele-
vated portions of Guatemala, Nicaragua, and Hon-
duras were isolated from major portions of Mexico
by the Isthmus of Tehuantepec. With no endemic
Mexican species, the Dieffenbachia flora reveals
less endemism than does Anthurium (Croat, 1983a)
or Philodendron (Croat, 1997). Both Mexican Dief-
fenbachia are relatively widespread, with D. oerste-
dii ranging to Panama (Fig. 29) and D. wendlandii
Fig. 28).

Costa Rican. and

ranging to Panama (

The remaining
species not already discussed above appear not to
have strong affinities with South American species
and clearly do not have affinities with other Central
American species. On the other hand, there are
some, relatively few, Central American
among them D. killipii, D. nitidipetiolata, and D.
that are likely to be of South American

Panamanian

species,

tonduzit,
origin since they are wide-ranging species in South

America.
HORTICULTURAL SIGNIFICANCE

Dieffenbachia, like many other members of the
Araceae, is one of the world’s most important or-
namental plants. Owing to the attractive leaves and
hardiness under the difficult conditions found in-
doors, Dieffenbachia remains one of the most im-
portant ornamental plants in homes, offices, and
professional displays. Ornamental aroids play a ma-
jor role in the foliage-plant industry in the United
States, making up about one-third of total foliage
plant sales (Henny, 1988). Dieffenbachia is one of
5 aroid genera routinely among the top 10 foliage
a le in annual sales volume (Henny, 1988).
Araceae hold 7 of the top 13 positions in
terms “of overall sales in North America, including
the first two (R. Henney, comm.). An orna-
mental cultivar of Dieffenbachia is the second most
important in sales, and the genus consistently has

pers.

one or more taxa on the list of most popular orna-
mental plants in North Dieffenbachia

breeding and culture plays a major economic role

America.

in the United States in Florida, California, and Ha-
wall.
TAXONOMIC TREATMENT
ы es Schott, Wiener Z. Kunst 3: 820.
TYPE: Dieffenbachia seguine (Jacq.)
Vd

Seguinum Raf., Pl. Tellur. 3: 66. 1836 [1837]. TYPE:
guinum oe Raf. |= Dieffenbachia seguine
hott].
D. A . Bull. Torrey Bot.
TYPE: guirea VE aen
= [Dieffenbac us кш, . E.

Jacq)
Maguirea A Club 75: 635.
1948. s A. D. Hawkes

Terrestrial; caudices thick, often elongate and
prostrate, rooting at the lower nodes, the older por-
tions of the stem trailing across the surface of the
ground, often for considerable distances; sap often
milky and frequently with varying concentrations of
oxalic acid, with conspicuous annular leaf scars.
Petioles elongate, amplexicaul, sheathed to the mid-
dle or sometimes to the apex: sheath unequal and
often free-ending at apex; leaves clustered in a tight
whorl at the stem apex; blades ovate to oblong-
ovate, elliptic, oblanceolate, or obovate, acuminate
at apex, acute to obtuse to rounded at base, typi-
cally subcoriaceous, sometimes variegated through-
out or in areas along the midrib with paler colors:
midrib raised on both surfaces; primary lateral
veins pinnate, usually sunken above, raised below,
much more prominent than the minor veins, all lat-
eral veins extending to the margins without forming
a single collective vein but with several primary
lateral veins often forming a series of short, discon-
tinuous collective veins; interprimary lateral veins
sometimes present; minor veins distinct to obscure,
usually not markedly raised, sometimes connected
by transverse tertiary veins. INFLORESCENCES
shorter than the leaves, 1 to several per axil; bracts
short and usually inconspicuous; peduncle usually
somewhat flattened and angular with one edge nar-
rowed: spathe oblong, persistent, convolute at base,
often somewhat constricted about midway, opening
usually only above the middle, usually green on
outside, somewhat paler within; spadix slightly
shorter than the spathe, divided into pistillate and
staminate portions, each with naked unisexual flow-

ers; the pistillate portion basal, about as long as the
staminate portion, fused to the spathe, remotely
many-flowered (typically 20 to 80 rarely to 160):
white, free from the

staminate portion clavate,
often separated

spathe, densely many-flowered,
from the pistillate portion by a naked interval. Sta-
minate flowers consisting of 4 stamens united into
a 4- to 5-suleate, truncate synandrium: anthers lat-

Volume 91, Number 4 Croat 685
2004 Revision of Dieffenbachia

eral. contiguous, the common connective thick, sessile, depressed globose to depressed ovoid, 2- or
fleshy: the thecae obovoid to oblong-elliptic. des 3-lobate: ovules 1 per locule. pale green, semiglos-
hiscing by short, apical, pore-like slits: pollen ex- ху, erect, anatropous: placenta axile to basal: stylar
truded in strands, inaperturate, ellipsoid or oblong region inconspicuous; stigma large, hemispheric or
or nearly spherical, large, averaging more than 75 2- or 3-lobate, about as broad as the ovary, yellow
pm, exine psilate to obscurely verruculate and/or to orange in color. INFRUCTESCENCE with fruit-
sparingly punctate-foveolate to densely foveolate: ing spathe often turning yellow, orange, or red,

—
—

pistillate flowers moderately dispersed but often in breaking up longitudinally fruit to expose the
weak rows with 1 to 5(6) pistils per spiral, and colorful berries; fruits baccate. globose or 2- or 3-
surrounded by 4 or 5 claviform white staminodia, lobed, 1- or 2(3)-seeded: seeds globose or ovoid.
these longer than the ovary usually 2-5 mm. usu- the testa thick. smooth. green to blackish green:
ally spreading, sometimes fused briefly at the base: embryo large: endosperm lacking.

ovaries 2- or 3-carpellate, sometimes |-carpellate. Chromosomes 2n = 34, 68.

KEY TO DIEFFENBACHIA OF MEXICO, CENTRAL AMERICA, AND THE WEST INDIES
Га. Petiole involute, extending to base of blade and frequently prolonged beyond the base of the blade.
2a. Larger leaves regula dy to more than 45 em long and 23 em wide, cuneate at base, coriaceous, usually
glossy above. not variegated, uniformly green,
За. Petiole sheath markedly undulate, at least near the base; Atlantic slope.

la. Leaf blades matte and somewhat velvet ly to glisteningly velvety above, minute ‘ly wrinkled
on upper surface: drying dark blackish brown to dark vellowish беа aave: Atlantic sk ope
of Panama o0 . D. panamensis Croat

tb. Leaf blades semiglossy to glossy above and smooth on upper surface; үе medium gray
to dark brownish gray above, paler and yellowish gray to pale yellow- brown below
C ð a ERN ). standleyi Croat
3b. Petiole sheath not markedly undulate: Pacific slope 13. D. Көне hii Croat & Grayum
2b. Leaves rarely more than 45 em lone or 23 em wide.
oa. Primary lateral veins 6 to

( per side: known only from the type locality in the Panama Can
І

ü СОЕ A a ee ИНОНИ 22. D. p Engl.
5h. | Pr rimary lateral veins usually 15 or more
еа blades with primary late sd veins (10)15 to 17 per side; blade base obtuse to rounded:
blade surface glossy to moderately glossy. not at all bullate, rarely E d; petiole usually
1 a whitish band on the abaxial surface: Panama 6. D. . Croat
Ob. Leaf blades with primary lateral veins usually more than 18 per side; usually cordulate
base, usually matte and subvelvety above, usually bullate, often variegated: petiole lac ae ,
а whitish band оп the abaxial surface: Nic aragua to C ieee

=

ounce . D. tonduzii Croat & Grayum
Petiole sheath erect to A e endi short of blade base (exce " бар оп upper leaves).
Unsheathed portion of petiole usually triangular in cross section, sharply keeled to ridged abaxially.
the margins thickly winged . aurantiaca Engl.

FE:

7b. Petiole isang sheath subterete, rounded abaxially. with margins 5 rounded to acute е winged).
8 ея with petioles or major veins of lower blade surface minutely granular- puberulent to pu-
rulent.
9a. Primary lateral veins 23 to 36 per side, departing midrib usually at about a 90° angle:
midrib and primary lateral veins conspicuously Anian nt mn whitish trichomes
„%%% ͤœ—ůà3] PN . D. beachiana Croat & Grayum

9b. Primary lateral veins usually less than 18 pairs (rarely to 2 in D. grayumiana) usually
de а midrib 40°—60° at us midpoint; midrib and primary lateral veins inc onspicu-
ously granular-puberulent.

10a. Blades narrowly oblanceolate, 6.4 times longer than wide, less than 6 « cm ич
m opensts Croal

10b. Bee elliptic to hoa рие. oblong elliptic, to narrowly oblong- ен e D ate (rare у
narrowly oblanceolate in D. Кйшй}, 1.7-5.2 times longer жы wide, cm

w
=
=

ide.
Па. Petioles with sheaths ending no more than 5 em from base of e
FF . D. standleyi Croat
IIb. Puticles with "m aths ending more than 13 cm Boh v of 75 x
12a. Primary lateral veins arising at 30-40" angle; central Panama

ене رفا ت ب تسد م ین تاو‎ дыйкандардан 0. D. galdamesiae Croat
120. Pr rimary Ai veins arising at mostly 55705 (to 80° in D. grayumiana):
costa Rica and western dx nama.
Za. Plants usually stout. 1.5 m tall: blades narrowly ovate. (22) 30-54

em long. 10-32 cm "uh 1 36 X 18 cm). 1.5-2.6 times

686 Annals of the
Missouri Botanical Garden

longer than wide; Costa Rica to western Panama, 0-1300 m but most-
11. D. grayumiana Croat

у near sea leve
13b. Plants medium-sized, rarely more pa А т tall, usually s blades

mostly narrowly Pre lanceolate, 15-33 cm long, 4.2-13 cm 9
(averaging 21 X 6.8 em). 2-6.3 times К gi wide; Pan
(Chiriquí), 900-1600 т 3. D. ed n roal

8b. : "se with petioles or major veins of the lower blade surface glabrou
la. Petiole sheaths decurrent apically (lacking prominent Sade extensions); Atlantic low-

lands.
15a. Blades drying blackened; Panama (Bocas del Toro), near sea level —— г.
— : 9. D. fosteri Croat
15b. Blades "m sellowish Brown. greenish to vellowish brown.
16a. Petioles very glossy, drying as if covered with shellac; Nicaragua to Ecuador —
Menem 18. D. 5 Croat
16b. Pe stioles not dna: not drying as if covered with ss Па
Ta. Plants less than 1 m tall; blades usually less bon 10 cm wide
e 12. D. hammelii Cı roat & Crayum
17b. Ste de s usually more than Im ‘tall: blades more than 10 cm wide.
'etioles matte; leaf blades usually subcordate at tw. usually flecked
with creamy yellow — . D. grayumiana Croat
18b. жеө se miglossy: leaf blades cuneate to dus d or truncate at
base, usually plain green (rarely ipis with pale green).
19a. Petioles terete; sheaths decurrent at apex, tightly inrolled with
one side completely hidden b the other; Mexico to 1 кн
= primarily on Pacific slope pom in Oaxaca and Ver
2

1 Atlantic slope) 6. D. wendlandii Se ‘hott
19b. Petioles usually obtusely sulcate, sometimes ith an ob-
tuse medial rib; sheaths pa n margins erect; Nicaragua to
Colombia ny О "Engl. & K. Krause

14b. age sheaths (at least on one side) rounded to auric um al ap
ades with more than 18 primary latera veins or d primary lateral veins obscure,
pe more conspicuous than inte rprimary ve
21а. West Indian and South American species; or with both nre sulcate Pu
ioles and a thickened, prn spadix; fruits 2- to 3-lobed
А D. seguine (Jacq.) Schott
21b. Mainly Central American species (D. Mi D. bulimia, and D. obscurinervia
also in South America).
22a. Blades with 10 to 13 pairs of primary lateral veins, these moderately in-
conspicuous, barely more obvious than interprimary veins; petioles and
lower midribs with pale spots; Central Panama to C ee
es 19. D. obscurinervia C roat
22b. Blades with 18 to 28 pairs of primary 2175 veins, pe idedly more con-

=

spicuous than the interprimary veins: petioles and lower midrib lacki: ng
spots; Costa Rica, Golfo Dulce region . . burgeri Croat & Grayum
20b. Blades variously shaped, matte to glossy above, with 8 to 18 primary lateral veins per
side.
23a. Maris lacking medial sterile region, the male and female regions contiguous or
nearly so.

24a. D "p usually solid green, not densely and conspicuously pale-maculate.
Blades with major veins on the lower surface granular-puberulent -- =

D. lutheri Croat‏ .17 ی
25b. Blades with major veins on the lower surface glabrous 8‏

ехе 15. D. kis Croat

24b. райга densely and Pe — one mac ailai
26a. Stems more than 1 cm thick; petioles never pale- -mac A primary
» veins usually Е midrib at less than pe sta Rica
a Peninsula), Panama, and Colombia D. killipii Croat
26b. т. usually less than | cm thick; petioles ; distinc tly pale. maculate;
ee lateral veins usually departing midrib at 90° or more; Costa
Rica, Sixaola region, Panama, and Colo mbia Md
е da Ж Croat & Grayum
23b. Spadix їй. an evident medial sterile region, pistillaie and staminate portions
separated by a distinct naked spadix axis
27a. Plants usually less than 0.5 m tall... 20. D. oerstedii Schott
27b. Plants to more than 0.5 m tall.
Blades drying dark brown to blackened on upper surfac
29a. Blades usually with posterior lobes; lower blade 8 e drying

d

-]

Volume 91, Number 4 Croat 687
2

004 Revision of Dieffenbachia

a brown to yellowish gray-brown to dark yellow-brown

ellowish green; stems solid dark green, drying glossy and
minute aly 8 (the areoles interspersed with raphide cells):
Panama, Bie bo Province and the Azuero Peninsula in the
west (at 700—900 m in Herrera and Los Santos Provinces) to
Darién Province in the east, and to Colombia 50-800(1000) m

"er dC 14. D. ийла Сгоа!

29b. Blades lacking posterior lobes; lower bl: ade surface drying gray
ish black; stems UAE d dark green, drying smooth with a еф
ayer of raphide cells (but not minutely wrinkled); irre Bo-
ға Того, ѕеа ея vel

OST OOD . fosteri Croat
28b. Blades drying yellowish green to dark gray-green, rare i оа оп
upper surface.
30a. ШУ usually white at base: blades usually ^ 'ss than 20
J ). а Se ‘hott
30b. Pe ile 's not whitish at base. frequently paler dui stem but not
markedly paler than the remainder of the petiole; blades usually
more than 20 em long.
3la. s tioles usually sharply C-shaped, disc olore d and whitish
the base: blades matte

=

Я د‎ Schott
31b. a etioles terete to obtusely С -shaped or ива ly D-shape
not sharply sulcate, по! discolored and whitish at E

ssy.

32a. Species of mostly dry habitats in western Central

rica (Mexico to Panama): blades subcoriaceous.

semiglossy on upper surface, (15)20-55(05) em long

(averaging 35 X 17 cm); 75 to 200 m in eleva

›. D. w 1 ire 5с ‘hott

32b. Species of wet 4 habitats, -southe astern Nicaragua and
along the entire Atlantic slope and the Osa Penin-
sula of Costa Rica; blades moderate к, coriaceous
glossy on the upper surface, 16-36 cm long. (aver-
aging 23 X 12 ст); sea level to 200 m. mostly at
less than 100 m in elevation

>
=
=

N
xX

m 4. D. concinna Croat & бакша

1. Dieffenbachia aurantiaca Engl., Anales Inst.
Fis.-Geogr. Nac. Costa Rica 9: 209. 1898.
TYPE: Costa Rica. Puntarenas: "in silvis pro-
pe Santo Domingo ad sinum dulcem [Santo
Domingo de Golfo Dulce], fructif. Mart. 1896,”
A. Tonduz 9961 (holotype, BBI: isotypes. CRI.
US). Figures 2, 27A

ending and obliquely rounded to rounded-auricu-
late distally: unsheathed portion 0.5-2 cm long.
angular to + triangular in cross section, flat to
broadly sulcate adaxially (sometimes with a medial
keel). adaxial margins thin and revolute. acutely
keeled abaxially. abaxial margins thickly winged,
sometimes with a medial keel, thin, revolute, some-
Sour E OCS fetid and М times medially keeled at margins; blades oblong-
Stout herb, 0.7—2.3 m tall: sap fetid and caustic: de ИР ; |
lalis Gack i xu " E M ae de ‘Aide: elliptic to ovate-elliptic, slightly inequilateral. one
D b € € a c LI ` . ~ . .
| Ма ; side 1-1.5 cm wider than the other side, usually
portion reclining and up to 2 m long; internodes | i E
ә 0-4(6) n long. 5 7(10) adam A subcoriaceous, acuminate to abruptly acuminate at
em long, 5-7 c am., dark green te 7
+ © г Hd = r € ^. n ч re
pale green, semiglossy to glossy, streaked with paler Apex. slightly inequilateral and obtuse to rounded
айий: petiale 15-2549) cm lone iN or subcordate (rarely attenuate on one side) at base.
green: petioles 13-33(48) cm long (averaging 24 m "О І he
Я . ЫЕ | . (26)31-57 X 11-27 cm (averaging 39 X 19 cm).
long), C-shaped at base in cross section, moderately х | í h e 5
spongy, medium green, semiglossy adaxially, matte 1.1-2.6 umes auge an wide (averaging ш
and acutely l-ribbed abaxially, the surface finely ranging from about as long as petioles to 2.8 times

dark striate, sometimes variegated with paler green longer than petioles (averaging 1.7 times longer):

markings, sheathing % to nearly throughout (35%— margins weakly undulate; upper surface dark
97% their length and averaging 77%); sheath 6.5— green. concolorous or sometimes variegated, drying
25.538) em long (averaging 17.7 cm). medium dark olive-green to medium gray-green, weakly
green, finely dark green striate, sometimes varie- glossy to semiglossy: lower surface moderately pal-
gated with paler green markings. adaxially acute er, matte to weakly glossy, drying pale yellowish
margins sometimes much paler, with margins in- green: midrib flat to broadly concave above (broad-

curled but usually not overlapping, the apex free- ly sulcate near base), 5-20 mm diam.. sometimes

Annals of the
Missouri Botanical Garden

$ mm
—

Figure 1.
inner surface of spathe (Croa nce at anthesis showing fully
opene ү spathe with beetles in rl se of ы le and partially eaten sterile staminate flowers (Croat & Zhu 7665.

C. Dieffenbachia ven dlandii close-up of inflorescence showing intact unilocular pisti ils with mostly eaten staminodia
(e mons "e spathe tube partially removed) (Croat 39749). —D. Dieffenbachia M mature infructescence showing
exfoliated spathe and berries on wed out for display (Croat & D. Hannon 6553

\. Dieffe eal е а blade showing open position at anthesis with thrips present on
& Zhu 77042

K Z —B. Dieffenbachia tonduzii, infloresce

Volume 91, Number 4
004

Croat 689
Revision of Dieffenbachia

whitish, faintly striate above, bluntly acute to V-
shaped (a continuation of the triangular petiole) be-
low, drying brown below, faintly striate: primary lat-
eral veins (8)12 to 14 per side, departing midrib at
a steep angle, spreading at a 507-70? angle. grad-
ually spreading in a broad curve, slightly to mod-
erately paler than surface in the proximal one-half,
weakly raised to convex in valleys, flat and darker
than surface toward margins, drying mostly paler.
sometimes darker than surface above, weakly con-
vex and slightly paler than surface below. drying
yellowish and paler than surface or brownish and
darker than surface below: interprimary veins pre-
sent or absent, usually with 1 between each pair of
primary lateral veins in the lower % of the blade:
minor veins darker than surface. visible but mod-
INFLORESCENCES to 3

рег axil; peduncle (7)10-18 em long, acutely an-

erately obscure. below.

gular on one side, drying striate, 3-6 mm diam.:
spathe 17—25(38) em long. 223.5 em wide, flatten-
ing lo 5.7-8 em wide on tube, 2.5-6.5 em wide al
constriction, 34.3 cm longer than the spadix. grad-
ually long-tapered toward apex from the middle.
uniformly light green to medium green throughout:
weakly glossy outside, glossy inside: spathe blade
2.5-7 em wide when flattened: spadix 16—20(33)
em long: free portion to 15.5 em long: pistillate
portion 6.5-8.5(15.5) em long. 1.5-2 cm diam.
throughout (mostly drying 6-9 mm diam.): fertile
staminate portion 712.5 cm long, white, tapered
toward apex and weakly tapered slightly toward
base; intermediate sterile segment 1.54 em long.
with a few scattered pistils in lower half and a few
scattered staminodia in upper half: pistils 51 to 72.
irregularly scattered, with 3 to 4(6 to 7) across the
width of the spadix, separated from one another by
% to 4.0 times their width, depressed-globose, to 2

mm long, 1.2-1.6(2.8) mm diam..
2 mm

pale g green: stig-
2.5-3
wide. white; staminodia 3 to 5 per pistil, 1.5—2(3.8)

mas cushion-shaped, high, mm

mm long, free or briefly united at base, held well

above the stigmas sometimes united for much of

their length; synandria 1—2(3.4) mm diam., margins
irregularly angled with rounded, linear to 3-sided
slit medially at apex. INFRUCTESCENCE 19-24
em long: spathe orange outside; spadix 8-15 cm
long: berries red-orange, В & К yellow-red 6/2.5 to
B & K yellow-red 7/5 to red B & К red 6/10 (Berlin
& Kay, 1969), subglobose, ovoid to ellipsoid, 7—10
mm long.

Distribution and habitat. Dieffenbachia auran-
tiaca is known only from southwestern Costa Rica
and adjacent Panama, in the region of the Osa Pen-
insula in Costa Rica and the Burica Peninsula in

Panama. It occurs in wet forests and swampy sites
from near sea level to 780 m in Tropical wet forest
(T-wf) and Premontane wet forest (P-wf) life zones
(Holdridge, 1967

Phenology. Dieffenbachia aurantiaca begins to
flower in the early rainy season with flower buds
having been seen as early as May and as late as
August, and mature open inflorescences seen be-
tween May and December. Fruiting occurs between
September and March.

Discussion. The species is characterized by its
more or less elliptic, usually unvariegated, green-
drying blades, obtuse to subcordate at base. but
especially by the triangular and weakly sheathed
petioles, decurrent at apex. It is probably most
closely related to D. horichii, but differs from that
species in having a longer free portion of the pet-

iole, which is more or less triangular. Also vege-

atively similar are D. longispatha and D. nitidi-
petiolata, but both differ primarily for the same
reasons, i.e., that the free portion of the petiole is
not triangular.

An unusual collection, Croat 67700, from a rel-
atively dry area on the Pacific slope of Costa Rica
(drier than the typical sites for this species), has a
petiole that is described as terete though the col-
lection otherwise matches D. aurantiaca. The col-
lection looks vaguely like D. nitidipetiolata. which
is otherwise found only on the Atlantic slope. A

londuz collection at US originally labeled Tonduz
9961, was relabeled 7177 despite the fact that it
was also collected in March 1896. It appears to be
specimens labeled Tonduz

identical to two other

9961, the type collection number.

\dditional specimens examined. COSTA RICA. 18XX.
Pittier & Dur rar = s (BR). Puntarenas: near
Norte. Allen 5 (UC ); Playa Blanca, Golfo Dulce. Val-
епо 462 (CR, de Golfo Dulce-Río Terraba, Skutch 532€
(Us): Cantón de Osa, Aires, Fila Retinto, from
Palmar Norte to Jalisco, Grayum ¢ 39 (C
)):

Palmar

~

Buenos

km S of Palmar Sur), Grayum et al. 7549 (MO); near 5705
Am Hwy. vic. Piedras Blancas, Croat 32955 ч A. INB,
МО); W side of Fila Gamba, ca. 6 km from А. чене,
Croat & Grayum 59906 (CR, MO); Cantón us Golfito, Par.
Corcovado, vic. Estación Sine ma, 14 Apr. 1995, Picado «e
Gamboa 138 я B. MO); Piedras Blancas-Rincón (on Osa
Peninsula), mi. W of Pan-Am Hwy., Croat 67700
(MO): S san = de Coto Brus to Ciudad Neily, NE slopes
of die de Cal. Hammel & Grayum 14169 (MO):
Norte-Panama border, 3 km N of turn-off 15 1 55 бп, i 5
«€ Hannon 79193 (COL, INB, MEXU, MO. UB. WU): ¢

2 km N of Chacarita, S of Palmar Norte. uu et al. 1
(IN B. MO, U). San EE N of Palmar Norte, trail to Jal-
isco, Croat 35210 (F, MO); 5 km W of Palmar Norte on
rd. to Puerto Cortes, Line 161 (F, NY, US); :
General-Dominica, ca. 1 mi. beyond divida, Croat 35292
(INB, MO). PANAMA. € hiriquí: Puerto Armuelles.
Woodson Jr. & Schery 861 (F, MO); Puerto Armuelles-San

San Isidro del

Annals of the
Missouri Botanical Garden

18 mm
DEE

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

Bartolo Limite, 7 mi. W of Puerto Armuelles, Croat 35079
(MO): Burica "rara 8 km W of Puerto 1

Croat 21961 (F. MO); кы Manzanillo, 9 km

of Puerto is S. Busey 743 (МО); Quebrada елы
banito beyond "s Represa, 2 mi. SW of Puerto Armuelles,
Liesner 114 (MO, US).

рә

Dieffenbachia beachiana Croat & Grayum,
Novon 9: 492. 1999, TYPE:
del Toro: Chiriquí Grande-Fortuna, 13.2 mi. W
of Chiriquí Grande, 8*45'N, 82*10'W, 310 m.
T. B. Croat & M. H. Grayum 60130 (holotype.
MO-323065!: isotypes Bl. Kl. PMA!, US). Fig-
ures 3, 28B

Panama. Bocas

Slender herb, 40-100 em tall; stems briefly
creeping at base; internodes 2-6 cm long, 1.5-3.5
em diam., medium green to olive-green, sometimes
streaked with cream, semiglossy and obscurely
roughened. LEAVES clustered near stem apex.
erect-arching; petioles 17-46 cm long (averaging
26.5 cm long). sheathed 25%-83% of petiole (av-
54%): sheath 10-22 cm long (averaging
14.2 cm), decurrent at apex; unsheathed portion

—

eraging

(2.5)10—30 cm long, broadly C-shaped in cross sec-
tion, dark green to brownish, flattened with acute.
erect margins or sharply to bluntly sulcate adaxi-
ally, surface pale green-mottled, matte, usually mi-
nutely roughened and with scattered scales, whitish
raphide cells visible, drying with scattered clusters
of pustular raised areas with granular-puberulent
protrusions; b/ades narrowly elliptic to lanceolate,
rarely narrowly ovate, inequilateral, one side I
cm wider than the other side, thinly coriaceous to
subcoriaceous, drying papyraceous, weakly bicolo-
rous, + equilaterally acuminate at apex (the acu-
men to 5 mm long), slightly inequilateral and acute,
rounded or truncate (rarely subcordate in Panama)
at base, 16—41 em long, б.5—15 cm wide (averaging
28 X 10.7 cm).
(averaging 2.6). 0.7—1.9 times longer than petioles

1.8—5.3 times longer than wide

(averaging 1.12 times longer than petioles): margins
crisped-undulate: upper surface dark green (in
Panama sometimes mottled with white or cream),
semiglossy (rarely matte), lower surface semiglossy
to weakly glossy or matte, slightly paler; midrib flat-
raised above, often striate, usually concolorous
above, convex to thicker than broad below, puber-

ulent with thick, whitish trichomes below; primary

lateral veins 23 to 30(36) per side. departing midrib
at a 70-110? (to 45? toward apex and sometimes
at base) angle, arising acutely then straight to
weakly curved to the margins (then sweeping prom-
inently toward apex), usually quilted-sunken above,
convex, puberulent with thick, whitish trichomes,
sometimes with adjacent veins alternating ascend-
ing and descending below; interprimary veins usu-
ally present, scarcely less visible than primary lat-
distinct and
INFLORESCENCES 1 to 3

per axil; peduncle 9-13 cm X 5-7 mm, drying 3—

eral veins; minor veins moderately

weakly raised below.

4 mm diam.; spathe 10—19 cm long, gradually con-

stricted at middle, gradually

long-tapered to apex; spathe blade to 3 em diam.

green throughout,

when flattened; spathe tube 1-2 em diam.:
13-15

drying 7 mm diam. throughout: fertile staminate

spadix
cm long; pistillate portion 4.5-6 cm long.

portion 5—6.5 em long. drying 4 mm diam. through-
out; intermediate mostly sterile portion usually 2—
3.5 cm long, 2 mm diam., sometimes with pistillate
and staminate portions almost contiguous: pistils 46
to 66(100). 2 to 4 situated across the width of the
1.5-2 X 1-1.6 mm;
stigmas subglobular, about as broad as the ovary:

spadix, ovary oblong-ellipsoid,

staminodia narrowly clavate, usually not at all fused
at base, ca. twice as long as pistil; synandria 1.8-
2.0 mm diam., margins irregularly subrounded,
drying smooth and light brown at apex. INFRUC-
TESCENCE with spathe (10)14—16 cm long. some-
what flattened, yellow-green mottled green and
white with darker flecking, maturing to orange: spa-
dix 6-10 cm long; berries orange, subglobose, 6-8
mm diam.

Distribution and habitat. Dieffenbachia beachi-
ana ranges from northeastern Costa Rica to western
Panama (Bocas del Toro, Chiriquí, and Veraguas)
at elevations of 40 to 800 m. In Costa Rica it occurs
on the Atlantic slope of the Central Cordillera and
the Cordillera Talamanca, ranging from the Sara-
piquí region to Tortuguero and Siquirt

Phenology. Dieffenbachia 3 initiates
inflorescences in the late rainy season with plants
anthesis in the

reaching dry (January

through April). Immature fruits have been seen

season

from April to September and mature fruits have
been seen from April to December.

e

Figure 2. Dieffenbachia aurantiaca (Croat 35292). I Habit, мом ореп inflorescence. —B. Close-up of spathe
and spadix (spathe held i splayed us m C. Clos E showing fully sheathed petiole. —D. Leaf
cluster with open spathe, showing de n view. —E. -up of portion of ie vith pistils showing stigmas and the

overtopping club- shaped staminodia. —F. Close- up 5 ptus pec of spadix showing strands of pollen emerging
la.

from between androeci

692 Annals of the
Missouri Botanical Garden

C

Figure 3. Dieffenbachia beachiana. —A. A series of leaves showing adaxial surface (Croat 44283). —B. Close-up
and a cluster of inflorescences (Sims 8). —C. Adaxial surfaces of leaves anc

of leaf cluster showing variegated leaves
open Td |). Class -up of inflorescence showing emergent portion of the e and adaxial surface of

petiole. C, D. (Croat 1 6844 ).

Volume 91, Number 4
2004

Croat 693
Revision of Dieffenbachia

Discussion. The species is characterized by its
moderately thin, quilted blades with many broadly
spreading primary lateral veins and erisped-undu-
late margins with the lower midrib and primary lat-
eral veins puberulent. Dieffenbachia beachiana is
similar to D. galdamesiae, a species from central
Panama that also has somewhat puberulent midribs
on the lower blade surfaces. That species differs in
having the pubescence much shorter, merely gran-
ular-puberulent, and has fewer than 22 veins per
side (vs. 23 to 36 for D. beachiana) that arise from
the midrib at a 30°-40° angle (vs. 70°-110°). In
addition, Panamanian populations of D. beachiana
their blades usually white- to

differ in having

cream-mottled, whereas those of D. galdamesiae
are always solid green in color. Dieffenbachia be-
achiana is also somewhat similar to D. grayumi-
ana, but that species differs in having the veins
merely minutely granular in slender rows on drying.
and in having somewhat more ovate and wider
blades.

A single collection (Croat 66953) from Veraguas
Province in Panama differs in having the primary
lateral veins curving more prominently toward the
apex than material from elsewhere in western Pan-
ama and Costa Rica. In addition, the pubescence
is merely granular-puberulent rather than puberu-
lent. Hammel 9660,
redia Province in Costa Rica, probably represents

collected at La Selva in He-

a hybrid between D. beachiana and D. concinna.
The specimen has the slightly scabrous petioles
and the impressed major veins of D. beachiana, but
the blades are more less elliptic and dry the
color of D. concinna.

Additional e seen. COSTA RICA. Heredia:
Rio Peje-Río Sardinalito, Atl. slope of baie: Barva. Gra-
yum гиа Mor San José-Pto. Меј f Chilamante.
11.6 mi. N of Cariblanco, Croat 68358 ( В. ^ R. MQ): Finca

(CR, F); Zona Protecto
Peje- Río oer ‘imo, Grayum & Show i 220 (DUKE). Li-
món: Río Pacuare-Quebrada Diablo, ca. 2.5 km E of Si-
quirres, Ca 760 8 A Par. Tortuguero, Est. Agua

‘fa, Robles 1234 (CR, МО); La Colombiana Farm,
United Fruit Co., anti 36840 (US). Puntarenas: Gol-
fito, Par. Nac. Esquinas, Quebrada 1 Sanchez 539
(MO). San José: жо ez de Coronado, Braulio Carrillo
NP, along hwy. San José to Siquirres, trail to Río S
NB, MO, WU). PANAMA.
Toro: Chiriquí Lagoon, Water Valley, von

) SW of Chiriquí Grande, Thompson 4937
(CM); Fortuna Dam- Chiriquí Grande, 7.3 mi. N of |
over Fortuna Dam, 3.2 mi. N of Continental Divide, Con
& Grayum 60255 (MO); an Grande-Fortuna, 7.7 mi.
W of Chiriquí Grande, 1.5 mi. W of Punta к йа, Croat &
Grayum 60094 (К, MO, ire near NN: Chiriquí
(я rande, McPherson 11816 (МО). Veraguas . of Santa

„ 8 mi. N of Escuela Circlo Alto de Piedra. Pise 66953
(Mo, PMA, SCZ, US).

M З 5 Costa Rica. Henny 5 (MO). =
redia: Fir a Selva, O.T.S. Field Station, originally co
e by po Bra: E хна" at Missouri Botanical sn
den (MBG), vouchered as Croat 59152 (MO).

3. Dieffenbachia burgeri Croat & Grayum, sp.
nov. TYPE:
Norte-Panamanian border, 3 km N of turn-off
to Rincón, 8°48'39"N, 83%16'18"W, 110 m. 10
Sep. 1996, J. B. Croat & D. Hannon 79211
(holotype, MO-5170493!; isotypes, AAU!, B!
CAS!, CR!, COL!, DUKE!, EAP!, F!, GH!,
HUA!, INB!, K!, M!, MEXU!, NY!, PMA!,
RSA!, US!, VEN!, UB!, WU!). Figures 4, 27B.

Costa Rica. Puntarenas: Palmar

р кү terrestris —] m; internodia 0.5-2.0 ст longa.
1.2-2.5(3.5) cm dn petiolus 13—48 cm longus,
atus jan longitudinis; vagina 8.5—20 em longs. inequi-
lateralis acute ad apicem apex; pars libera 5.3-29.5
longa; lamina oblongo- Eu. ai anguste elliptica,

cm longa, 5-16 cm lata, nervis primariis laterali-

bus (13)18-28 utroque; ini n ‘entia 1—7 in гыт ах-
ngus; spatha 11.5-
1.

vagin-

9 cnm

—

Ша: pedunculus 7.5-12 cm lor
cm longa; spadix 9-15. 6« cm longus; pistilla 21—3

Herb, 0.5-1
internodes glossy to semiglossy, drying frequently
0.5-2 cm 1.2-

2.5(3.5) em diam., dark green to blackish green,

tall, sap milky, sharply foetid:

matte and minutely warty, long,
drying dark brown to black or yellow-brown or yel-
low-green. LEAVES scattered along stem with areas
exposed except near apex; petioles 13-48 cm long
(averaging 26 cm long), dark green, surface some-
what mottled, weakly pale-streaked near base.
glossy to semiglossy, sheathing % to % the length
of the petiole (0.5 their average length); sheath 8.5—
20 cm long (averaging 12.6 ст), sometimes solid
creamy white, with margins often drying thin and
light
sheathed portion 5.3-29.5

brown, the tip inequilaterally acute; un-
cm long (averaging 12.9
em). variable in cross section, from subterete to C-
shaped or U-shaped, sharply sulcate to somewhat
flattened near apex adaxially, the margins obtuse to
acute; blades oblong-lanceolate to narrowly elliptic.
25—40 cm long,
10.5 em).
ing 2.8 times longer than wide), 0.83—1.6 times lon-
1.21

slightly inequilateral, one side 0.4-1.4 cm wider

5-16 cm wide (averaging 30.5
1.9—3.7 times longer than wide (averag-

times longer).

—

ger than petiole (averaging

than the other side, thinly coriaceous to subcoria-
ceous, slightly to moderately bicolorous, gradually
long acuminate at apex, narrowly acute to rounded
and equilateral or slightly inequilateral at base (one
sometimes up to 6 mm higher on the midrib than
the other); upper surface solid dark green, matte to
weakly glossy (sometimes variegated with pale mot-
tling), drying gray-green to dark olive-green: lower
surface slightly paler, semiglossy to weakly glossy

Annals of the
Missouri Botanical Garden

E
E
e.

>> «=

„= *

T^. »
E

n
„
ps

Es

6mm
Кес

@

Figure 4. Dieffenbachia burgeri. A, (
roots, stem, leaves, and inflorescences.
—C. Close-up of inflorescence with spathe cut open.

, D. (Croat & D. Hannon 79211). —A. Side view of whole plant showing
B. od & Grayum 59814). Cultivated collection with open inflorescence
—D. Mature infructescences, one open with berries expose dan

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

(sometimes matte or weakly glossy on both surfac-
es), drying medium yellow-green to yellow-brown:
midrib above flat to sharply sulcate, sometimes flat-
raised, 3—5 mm wide, semiglossy, concolorous, dry-
ing slightly darker than surface; convex to thicker
than broad below, convex toward apex, slightly pal-
er than surface, drying dark brown to yellow-brown,
often acutely 1-ribbed; primary lateral veins (13)18
to 28 per side, departing inidrib at an acute angle,

then spreading at angle,
along margin, not forming collective veins, sunken

sweeping

to quilted above, convex beneath, drying darker or
lighter than surface; the interprimary veins slightly
less prominent than primary lateral veins; minor
veins moderately close and darker than surface
(drying weakly raised); surface minutely speckled
on drying. INFLORESCENCES 1 to 7 per axil; pe-
duncle 7.5-12 cm X 4 X 7 mm, medium green,

moderately glossy (sap with a faint, unusual scent):
spathe 11.5-15(21) cm long at anthesis, 1.1—1.9 cm
longer than the spadix, glossy to semiglossy on both
surfaces, flattening 2.7-3 cm diam. at constriction,
dark green outside throughout, slightly paler inside:
spathe blade < 2 cm diam. when furled; spathe
tube to 10 em long, 1.5-2.0 ст diam., flattening
3.1-7 cm wide; spathe blade 2.7-3.7 ст diam. at
anthesis; spadix 9-15.6 cm long at anthesis; free

2

portion 4—8.7 cm long; pistillate portion 5-6 cm
long: the fertile staminate portion 4—6.5 cm long.
5-6 mm diam., directed slightly forward out of the
spathe: sterile intermediate segment 1.5—3 cm long.
5 mm diam.,

few just below fertile staminate portion; pistils 21

with many staminodia near base and

to 37, moderately closely spaced, almost contigu-
ous, to 3 dispersed across spadix width, weakly
constricted below middle, green to pale yellow:
stigmas pale yellow, 1-1.5 mm on drying: stami-
nodia about as long as or slightly longer than pis-
tils, somewhat flattened and thickly swollen, sub-
globular and somewhat truncate at apex; synandria
drying irregularly somewhat rounded, the margins
usually irregularly turned upward, 1—1.4 mm diam.
at apex, orange to yellow-orange, green, narrowly
angled on one side. INFRUCTESCENCE
spathe usually orange; fruiting spadix 5-7 cm long.
ca. 3 em wide: berries orange-red to red-orange dry-

with

ing pale yellow-brown, ovoid, 7-8 mm long: seeds
drying blackened, minutely warty.

Distribution and habitat. Dieffenbachia burgeri
is endemic to southwestern Costa Rica on the Pa-
cific slope from Dominical to the Osa Peninsula,
sea level to 500 m, rarely 1000 m elevation, in
Tropical wet forest (T-wf), Premontane wet forest (P-

wf), and sometimes in Premontane rain forest (P-rf)

life zones (Holdridge, 1967). It occurs in wet forests
and swampy sites.

Phenology. Flowering in D. burgeri occurs in
the late wet season to early dry season from No-
vember to March, and mature fruits have been seen
from early April to early October.

Discussion. The species is characterized by the
petiole sheathed 444 of its length, with the sheath
acute at the apex; and the usually matte, greenish-
drying leaf blades with numerous primary lateral
veins. The blades are quite variable, ranging from
narrowly oblong-elliptic to ovate-elliptic, oblong-
lanceolate or narrowly elliptic. Dieffenbachia bur-
geri is most easily confused with D. oerstedii and
differs from that species in having the petiole
sheath acute at the apex, rather than free-ending
and rounded to auriculate as in D. oerstedii. In ad-
dition, D. burgeri has more primary lateral veins.
numbering (13)18 to 28 per side (vs. (4)6 to 9(11)
per side in D. oerstedii).

Burger & Liesner 7254 describes the spathe at
anthesis as having a strong unpleasant aroma.

Etymology. The species is named in honor of
William. Burger of the Fie
History, long-time expert on Costa Rican plants,

d Museum of Natural

who made the first collection of the species as well
as most of the earliest collections during his ex-
peditions to Costa Rica.

Paratypes. COSTA RICA, Puntarenas: Palmar, Sur-
Chaci و‎ km 287, ca. 3 km NW of Chacarita, Grayum et
al. 7 (INB, MO); Refugio Golfito, Fila Gamba,
Río ха drainage, Grayum & G. Herrera 9236 (CR,

km S, З km W of Cañasas,
Croat & Grayum 59814 (COL, CR, INB. MO, PMA
i P ‚КН, US); Piedras Blancas Rincón 3.7 mi.
W a Pans niat Hwy., diei е MO); Chacarita-Rincón
de Osa, ca. 6 km Chac ‚ Croat & Grayum 59731
(CR, MO); Rincón is Osa, ridge hots (шык Aparicio-
Quebrada лш Сгауит et al. 4014 (CR, MO); W
oat & Grayum 59851 (MO): Dis Nac.
of Fila Gamba hills behind Esquinas
Rain Forest Lodge, along Quebrada Negra, at end of side
rd. off of Villa Bricena to Golfito Rd., Croat & D. Hannon
79286 (CM, INB, MO); San José, along rd. to San Isidro
del General, Burger et A 10671 (F. MO); Golfito, Que-
brada Negra, Marten 848 (Е); Osa, ca. 5 km № of Rincón
de Osa, Burger & эы Jr. 8898 (CR, F); near the aro
ca. 4 mi. W of Rincón de Osa, Burger & Stolze 548
W of airstrip, U XE & Utley 1100 (CR. F). San pi.
Pérez Zeledon Cantón, San Isidro General-Dominical, Fila
Tinamastes, Croat & D. Hannon 79112 (INB, MO, QCNE,
USM); San Isidro del General-Dominical, shove Alfombra,

Burger & Baker 10121 (Е, MO).

of Rincón de Osa, C
ctor Esquinas, vic.

un

4. Dieffenbachia concinna Croat & Grayum, No-
492. 1999. TYPE: Costa Rica. Puntar-
enas: Palmar Norte-Panamanian border, 3 km
N of jet. to Rincón, 8°48'39"N, 83%16'18"W,
110 m, 10 Sep. 1996, J. B. Croat & D. Hannon

von 9:

696

Annals of the
Missouri Botanical Garden

79191 (holotype, MO-5170498!; isotypes,
AAU!, B!, CAS!, COL!, CR!, DUKE!, F!, GH!,
HUA!, INB!, K! Ml. MEXU!, NY!, PMA!, US).

Figures 5, 28А.

Small, erect herb, 0.6—1.3 m tall, sap milky: in-
ternodes glossy, 1.5—4(7.5) em long, 1—4 em diam.
medium green to dark green, obscurely marbled
light to medium green. LEAVES erect-arching: pet-
toles 7.5-25(35) em long (averaging 17 cm long),
terete and obtusely sulcate near apex or subterete
to C-shaped or D-shaped in cross section, flat to
shallowly sulcate adaxially (the margins obtuse to
acute), rounded or sometimes acute abaxially, mod-
erately erect, semiglossy or almost matte, dark
green to olive-green, blotched striate or streaked
white or silver-green, drying green to sometimes
light yellow-brown, sheathing from lower 7, to near-
ly throughout (averaging 0.63 of length): sheath
0.7-13(20) cm long (averaging 9.5 em). to 1.5 cı

diam., margins erect to involute, the tip asymmet-

rically auriculate to rounded and free-ending, with
one side obtuse to rounded, with the other side
acute to obtuse; unsheathed portion 1-13 em long,
to 1.5 em diam.; blades usually + elliptic, ovate-
elliptic, rarely ovate or broadly lanceolate, 16-36
em long (averaging 23 em long), (7.8)10—15.5(20.5)
cm wide (averaging 12 em wide), 1.5-2.9 times lon-
ger than wide, broadest usually at or near middle,
0.8-2.4 times longer than petiole, equilateral to
slightly inequilateral, one side to 1 em wider than
the other side, equilaterally acuminate at apex, the
acumen sometimes apiculate, broadly acute or usu-
ally rounded, slightly inequilateral at base, mod-
erately coriaceous, weakly to moderately bicolo-
rous; upper surface semiglossy to glossy, dark green
or rarely white to cream or yellow-green splotched
or flecked, drying dark olive-green, dark gray-green
to yellowish brown; lower surface moderately paler,
matte to weakly glossy, green, rarely dark gray-
green, drying yellowish brown to green, rarely dark
gray-green; midrib flat to broadly flat-convex and
concolorous to paler than surface above (sometimes
paler in distal ! above), low-convex to convex or
rounded-triangular, slightly paler than surface be-
low, drying light brown to dark brown with medial
portion usually drying darker: primary lateral veins
6 to 12(14) per side, spreading from midrib at a
45*-70* angle (sometimes arising at an acute an-
gle), only rarely at different angles on opposite side
of blade, weakly sunken above, convex to obscurely
raised below: the interprimary veins sometimes vis-
ible, 1 between each pair of primary lateral veins;
minor veins indistinct to visible and darker than

surface below. INFLORESCENCES 2 to 8 per axil:

peduncle (2.5)8—17.5 em long (averaging 10.5 ст
long), somewhat compressed dorsiventrally in cross
section, 3—4 mm wide on drying: spathe 11—25.7
em long, 1.5-2.0 em wide when furled (as long as
or up to 2 times longer than peduncle and aver-
aging 1.6 times longer), constricted 4.5 em above
base, the constricted area 1.8-3 em wide when flat-
tened, medium to pale green outside, somewhat
darker on tube except white on open face, uniform-
ly paler within, drying dark brown to blackened
throughout; spathe blade 3.3 cm wide when flat-
tened; spathe tube 4.5-8.5 cm wide when flattened,
paler inside; spadix protruding forward at anthesis,
12-14 em long; free portion 6.5-9.5 em long; pis-
tillate portion tapered toward apex, 4.5-9 em X 5-
12 mm, stipe and axis pale green; fertile staminate
portion white, tapered slightly toward both ends, 8—
9 em long, 7—10 mm diam. midway; sterile stami-
nate. portion 2.54 cm long: mostly sterile inter-
mediate segment 5-7 mm diam., mostly bare but
with a scattering of staminodia on both ends (es-
pecially at base); pistils 42 to 65, closely spaced:
ovary globose, 1-2.5 mm diam., pale green: stigma
pale yellow; staminodia 1—5 mm long, up to 3 times
longer than pistil, somewhat flattened toward base
and free at base, tapering and somewhat globular,
1-2 mm diam. at apex: synandria with flowers ir-
regularly rounded, 0.8-1.4 mm diam. INFRUC-
TESCENCE with spathe yellow-orange to bright or-
ange outside; spadix to 6-8 em long; berries bright
red to orange-red, oblong-ellipsoid, to | em long, 8

mm diam.

Distribution and habitat. Dieffenbachia concin-
na ranges from southeastern Nicaragua along the
entire Atlantic slope to the Osa Peninsula of Costa
Rica, sea level to 200 m, mostly < 100 m, some-
times locally common in rocky sites along streams.
Phenology. Flowering in D. concinna occurs
mostly during the middle of the rainy season, from
July through November (rarely December), espe-
cially September and October. A cultivated collec-
tion at the Missouri Botanical Garden flowered re-
peatedly over a two-week period during late May
and early June. Collections with immature fruits
have been seen from December to March. Mature
fruits occur primarily December through June, es-
pecially January to May but with one fruiting col-
lection each seen in August and September.
Discussion. The species is recognized by the
glossiness of all parts of the plant; its relatively
small stature; moderately coriaceous, more or less
elliptic, weakly inequilateral blades; and auriculate
petiolar sheaths. It is most easily confused with D.
oerstedii, but differs from that species in its larger

Volume 91, Number 4 Croat 697
2004 Revision of Dieffenbachia

A
жч

Figure 5. Dieffenbachia concinna. VH, G. (Croat 78318). E. (Croat 67594). A. Close -up of adaxial surface of
blade. —B. Crown of plant with inflorescences. one open. —C. Close te of stem and petiole bases showing variegations.
—D. Close-up of opened inflorescence exposing e e spadix. —E. Close-up of inflorescence with portion of spadix
жы е pa staminodia overtopping pistils. Close-up of be showing emerging threads of pollen filling

athe. —G. Close-up of male portion of spadix s androecia with anthers exposec

698

Annals of the
Missouri Botanical Garden

size (to 1.3 m vs. 0.75-1 m in D. oerstedii), and
more coriaceous blades typically broadest at the
middle (vs. broadest below the middle in D. oerste-
dii) with more numerous primary lateral veins (6 to
12(14) vs. mostly 6 to 9 for D. oerstedii). In addi-
tion, the blades of D. concinna are glossy above
and almost rounded at the base versus weakly
glossy to matte and subcordate in D. oerstedii.
Grayum et al. 10588, from the headwaters of the
Río Piedras Blancas in Puntarenas Province, is un-
usual not only in occurring much higher (to 900 m)
than most collections of this species but in having
a broader leaf (to 19 em wide) with a longer petiole
(to 30 cm). In other respects it agrees with other
collections of D. concinna. Hammel 9660, collected
at La Selva in Heredia Province in Costa Rica,
probably represents a hybrid between D. beachiana
and D. concinna. The specimen has the slightly
scabrous petioles and the impressed major veins of
D. beachiana, but the blades are more or less el-
liptic and dry more the color of D. concinna. Croat
& Hannon 79199, collected south of Palmar Norte,
appears to be a hybrid between D. aurantiaca and
D. concinna. Its blade shape and maculations, and
numerous inflorescences suggest D. concinna, while
the broadly sulcate petiole favors D. aurantiaca.

Additional есы examined. COSTA RICA. Не-

redia: near Puerto Viejo 9 m near Río Sucio, ps
8 (MO), Croat 35702 ; Finca La Selva

Field Station on the Río Puerto ae o just E of its пк tion
with the Rio 5 Hammel 9688 (DUKE), Croat
78732 (INB, MO, W). Limón: La Colombiana Farm, Unit-
ed Fruit Co., p y 36739 (US); headwaters of Quebra-
da Mata de Limón, Finca Anai (Sixaola region), Grayum
el al. 4447 (MO); Cerro 5 due a la Barra de
Tortuguero, К. ae 2090 (CR, О), Barringer et
al. 1973 (F); Par. Nac. dh dud p est rito 7856
(CR); Boca de li e de Tortuguero, Burger & An-
tonio 11249 (F. MO); Pococi, Refugio de Vida Silvestre

Barra del Colorado, SE base of Cerro del Tortuguero, Gra-
yum et al. 11139 (CM, CR, INB, MO, USJ); Río Chirri-
pócito-Río Sardina, Refugio Nac. Barra del Colorado, Gra-
| R. MO); Río Reventazón, Finca Montecristo
below Cairo, Standley : Yale rio 48960 (US). Puntaren-
as: McAlpin 85-33 (SEL); 2 km NW of Chacarita, 30 km
S of Palmar Sur, Car & een 8119 (CR, INB, MO);
ridge betw. Río Riyito (valley of Laguna Chocuaco) &
Que qeu n gas, S of Cerro Rancho Quemado, Grayum
et al. 7567 (MO); Rincón de Osa Rancho Quemado, ca.
10 km 4 of main inni ón—Pto. Jimenez Rd., Croat & Gra-
O); Osa, 6 km W of Rincón, Grant &
Rundell 92- 01928 (CR, MO, US); near the airfield ca. 4
mi. W of Rincón de Osa, Burger & Stolze 5161 (CR, F):
Osa PROIN NW of airfield, ca. 5 km W of Rincón de
er & Liesner 7196 (CR, F, MO, PMA); Osa Pen-
US); Costena-Cruces, Río Pie-
uciana, Grayum

—

Osa, Bur,
fnsula, Nicolson 3393 (BM,

CR);
Dodge 10020 (F, MO); Palmar Nor te de (
(К UC, US); Osa Penfnsula, 4 mi. W of Rincón de Osa:

— —

Raven 21532 (F); Rincón de Osa, Quebrada Aparicio-
Quebrada Aguabuena, Grayum et al. 3982 (CR, МО); vie.
of Boscosa, at Quebrada ие па, Croat & D. ۰
79238 (COL, INB, MO, NY, КН, TEX, UB); S

tor Esquinas, vic. of Fila ris hills behind PL i
Rain Forest Lodge, along Quebrada Negra, at end of side
rd. off of Villa Bricena to Golfito Rd., Croat & D. Hannon
79291 (CM, DUKE, INB, MO, P); Refugio Nac. Golfito, 5
tributary of Río Cañaza, Grayum et al. 9250 (MO); W side
Fila Gamba, ca. 6 km from Golfito airport, Croat & Gra-
yum 59930 (CM, K, MO); Río Claro, 2.5 mi. SE of Golfito,
Croat Ж mos Orotina-Jaco, valley of Río G
Hotel Pink

Tárcoles, ede Ganado, vic.
Paradise, Га» 2 (INB, M( . Corcovado,
Monkey Woods, Kernan & Philips 831 Y R, MO); Lower

ree 748 . Sirena, Que-
sada 51 (IN 55, CR); D s de Osa, Estación
Biológica S RS , 834'N 1'W, 200 m, 2 Sep.
1993, К. Aguilar 2195 (CR, 1155 MO) 0-1 e W of park
readquarters at Sirena, Liesner 2871 O); Pan-Am
Hwy., Rincón, Croat & E Hannon 79167 (MO); Rincón-
Rancho Quemado, just S of iim ón near Río Rincón,
D. ie Ae (H NB, MEXU, MO,

QCA, RSA, WU); vic. Palmar oe Aen 56604 (F. UC);
Punta Banco, M. 1 et al. 257 (CR); Coto Brus,
Guaymí Reserve, river trail along Río Limóncito near jet.
of Villa Palacios school trail, Koshear 59 (CR); Golfito,
Refugio de Vida Silvestre, Marten 789 (CR); Carr. Inter-
am.-Sinaf, Fila Huacas, ca. 4 km NE (by ban at Las
Huacas (*Venecia"), Grayum & Evans 10156 (CR, МО);
Palmar Norte _ 0, Quebrada Benjamin, Grayum et al.
9962 (CR, . San José: above Palma , Croat
35108 (MO). NiC ARAGUA. Río San Juan: Res. Indio-
Maíz, Cafio el Tambor, branch of Río San Juan, Rueda et
al. 4070 (MO). Panamá: E to Puerto
Jiménez, Osa, 40 km W of Poss. Hwy., rt. 2, L. Gómez

Lookout nos

EI

Croat &

Y

d tions. Costa Rica. Puntarenas: Esqui-

‚ 25 km SE of Palmar Sur, along Pan-Am Hwy., orig-

inally сае by Bruce Me Alpin (Selby 85- 33), 25 m,

994, cultivated at MBG, vouchered as Croat
77281 (MO); 15 May 1996, Croat 78318 (MO

N

Dieffenbachia copensis Croat, sp. nov. TYPE:
Panama. Coclé: El Copé, forest on Continental
Divide above El Copé, 8°38'N, 80538 W, 700—
900 m. 27-29 Apr. 1985, B. Hammel 13636
(holotype, MO-3284876!). Figures 6, 27B.

5

rba 45 cm alta; internodia 7 mm longa, 7 mm diam.,
petiolus (17)21-29.5 cm longus, vagina 8-12.5 cm longa;
pars libera 10.5-15.5 cm longa; га anguste oblanceo-
ata, 25.5-33.3 cm longa, 5.2 cm lata; nervis primariis
ateralibus 9-12 5 infloresce ета 1 per ахШат; pe
.7 cm longa, 1.2 cm lata;

dunculus 5 cm longus; spatha 15
spadix 12.3 cm longus.

internodes about as
drying matte, dark

Small herb, to 45 cm tall;
long as broad, 7 mm diam.,
brown, finely and irregularly folded; petioles
(17)21-29.5 ст long, sheathed 41% 50% their
length; sheath 8-12.5 cm long, narrowly acute at
apex, drying dark brown to medium yellow-brown;
free portion 10.5-15.5 em long, subterete, obtusely
drying medium yellow-brown to dar

0

sulcate,

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

699

PANAMA
raceao

Dieffonbachla copense Croat
Prov.

El Cop

above to

COCLE
e.

8*-58'N, 80*-38'W,
700-900 m

Terrestrial

On slope In frst. Lvs
gree
Impressed ab

vy

MISSOURI
BOTANICAL GARDEN
HERBARIUM

N2 3284876

Forest on continental dvd
мп.

wa on mrgn drk
n above, pale secondary velns
ove,

Apr/27-29/1985

„ Hammel 1363

B 6
MISSOURI BOTANICAL GARDEN HERBARIUM (MO)

Figure 6. Dieffenbachia copensis (Hammel 13636). Type specimen.

Annals of the
Missouri Botanical Garden

brown, minutely granular to somewhat scabridu-

lous; blades narrowly oblanceolate, 25.5-33.3 cm
long, 5.2 em wide, 6.4 times longer than wide, nar-
rowly long-acuminate at apex, narrowly attenuate at
base, dark green and matte above, moderately paler
and semiglossy below, drying dark gray-green and
minutely granular above, light yellowish gray be-
low: midrib concolorous and narrowly raised above.
convex and granular-puberulent to hispidulous and
slightly darker below: primary lateral veins 9 to 12
pairs, arising at an acute angle then spreading at
457-50? angle, prominently curved upward along
the margins and extending to above the origin of
the next higher veins, paler and weakly sunken
above, convex and slightly darker below, drying
narrowly raised and granular; minor lateral veins
weakly visible; cross-veins equally visible on lower
surface: lower surface moderately granular. INFLO-
RESCENCE solitary, longer than the petioles: pe-
duncles 5 em long, drying 2.5 mm diam., pale yel-
low-brown: spathe 15.7 em long, 1.2 em diam., pale
green, drying medium yellow-brown, narrowly long-
acuminate at the apex (acumen 1.7 em long): spadix
12.3 em long; free portion 8.5 em long; pistillate
portion 5 em long, 4-5 mm diam.: staminate portion
5.5
mostly naked; intermediate sterile portion 1.1 em

cm long, 4 mm diam., drying yellow-brown:
long, 2.5 mm diam. on drying, with only a few sta-
minodia scattered throughout its length; pistils 38,
2 to З situated across the width of the spadix; ovary
0.5-6.0 mm diam.:
ovary; staminodia 2 to 4 per pistil, 1-1.4 mm long.
slightly thickened toward the apex, not at all broad-
ened toward the base; the sterile male flowers in 2

stigmas about as broad as the

rows, somewhat separated. from the fertile flowers:
synandria 2.2-2.8 mm long, 1.6-2.0 mm wide, ir-
regularly rounded to rhombic at apex. INFRUC-
TESCENCE not seen.
Distribution and habitat. Dieffenbachia copen-
sis is known only from the type specimen in the
Coclé Province of Panama at 700 to 900 m in the
Lower montane rain forest (LM-rf) life zone (Hold-
ridge, 1967).
Discussion. The species is characterized by its
narrowly oblanceolate, narrowly long-acuminate
blades with densely granular primary lateral veins
and a granular-hispidulous midrib on the lower sur-
face. The species is somewhat similar to both D.
galdamesiae and D. fortunensis, differing from both
in having proportionately narrower blades that are

| contrast, the

broader well above the middle. I
blades of D. fortunensis are broadest well below the
middle and have the pistillate and staminate por-

2

tions of the spadix contiguous or nearly so (vs. :

free section to 1.1 em long in D. copensis). Dieffen-
bachia galdamesiae differs in having blades pro-
portionately broader, 2.7—4.2 times longer than
wide, versus 6.4 times longer than wide in D. co-

pensis.

6. Dieffenbachia crebripistillata Croat, sp. nov.
TYPE: Panama. Coclé: Alto Calvario, above El
Copé, ca. 6 km N of El Copé, Atlantic slope
along trail which leads down to Las Ricas, Li-
món & San Juan, 8°39'N, 80736' W, 710-800
m, 22 June 1988, J. B. Croat 68746 (holotype,
MO-3610884!; isotypes, B!, CAS! COL!
DUKE!, F!, GH!, HUA! INB!, KI. MI. MEXU!,
NY!, PMA!, US!). Figures 7, 27A

denis 30—100(120) em alta: dnte поа 2.5—4 em longa,

5 365) em diam.; petiolus 7.5-24 cm longus: lamina
к el raro eee a vel oblong-elliptic a, (22)27
16(55) em longa, 10-25 cm lata, 1 s primariis late al
ibus (10)15—17 эбе! 1705 scentia 1-2 per ахШат;

en ulus (8.5) 10-14 em longus: sey 13-28 cm lon-
cm longus; parte pis-
mm lata.

ga, 2.0-3.2 em lata; spadix 13—
uliata б—10(12) em longa, 8-12

Short, thick-stemmed herb, 30-100(120) em tall;
sap foul-smelling, eventually turning white: inter-

2

nodes dark green, glossy, 2.5—4 cm long. 1.5—3(5
em diam.; petioles 7.5-24 cm long (averaging 16
em long) somewhat spongy, solid dark green or
with a white band on the abaxial surface, conspic-
uously sheathed ranging from 0.7 to fully through-
out the length (but rarely ending more than ] em
below the blade and often extending bevond the
base of the blade); sheath to 1.5 em high, 7.5-19.5
em long, inequilaterally rounded to auriculate at
apex; unsheathed portion usually not apparent but
when present 1—7 cm long (averaging 1.6 cm long),
broadly sulcate, the margins sharp: blades ovate to
rarely elliptic or oblong-elliptic, (22)27—46(55) cm
long. 10-25 cm wide (averaging 37 X 18 cm), 1.5-
3.3 times longer than wide (averaging 1.9 times
longer), 1.9-3.7 times longer than petioles (aver-
aging 2.3 times longer than petiole), somewhat in-
mod-

equilateral, one side up to 0.5-2.7 em wider,

erately coriaceous, abruptly acuminate and
downturned at apex, obtuse to rounded at base, the
basal portion of the blades held somewhat erect;
upper surface glossy to moderately glossy, usually
dark mottled with pale
green. slightly bicolorous; lower surface glossy. pal-
v; midrib flat-raised to flat-rounded and paler es-
pecially near base, 12-20 mm wide, becoming ob-
tusely convex toward apex and diminishing before

solid green sometimes

^

reaching the apex above, broadly flat-rounded to
narrowly rounded and pale green to white below
(especially near the base): primary lateral veins

Volume 91, Number 4 Croat 701
2004 Revision of Dieffenbachia

Figure 7. Dieffenbachia crebripistillata (Croat 75172). —A. Potted plant with open inflorescence (Croat 751 7.
B. Close-up of crown o m vith open inflorescence. —C. Close-up of inflorescence with pollen emerging 3 —
androecia (Croat 49243). —D. Close-up of иран scence eer tube flared out and spathe blade recurved. —E. Close-

up of inflorescence showing a. portion, interme diate sterile section, and lower section of staminate portion.

702 Annals of th

Missouri Botanical Garden
(10)15 to 17 per side, sunken to weakly sunken been made during the late rainy season (August—
above, raised below; interprimary veins obscure December).

minor veins mod-
erately distinct on lower surface. INFLORES-
CENCES 1 to 2 per axil; peduncle (8.5)10-14 cm
long, flattened laterally, pale green: spathe 13-28
em long, 1.3-1.5 times longer than peduncle, pale

above, obscurely visible below;

to medium green outside (sometimes white at an-
thesis), paler within, unmarked, + oblong, acumi-
nate at apex, only weakly constricted midway (con-
stricted area to 3.2 cm wide when flattened); spathe
tube 1.5-3 cm wide when furled, 8-8.5 cm wide
when flattened; spathe blade to 2.0-3.2 cm wide
when furled; spadix 13-26.5 cm long (averaging 18
em long), the free portion 8.5-11 ст long; pistillate
portion 6—10(12) em long. 8—12 mm wide; fertile
staminate portion 5-9 cm long, 6-10 mm diam.:
the mostly sterile intermediate portion (1)1.5-2.5
cm long, with some sterile male flowers in the up-
per Y; pistils (57)80 to LOO, scattered, frequently
adjacent, up to 5 in a row across the width of the
spadix, never more than 5 mm apart; stigmas pale
orange, densely pubescent; staminodia white, + ob-
long, ca. 2-3 mm long. rounded at apex; synandria
irregularly rounded at apex. smooth or weakly dim-
pled medially, to 2.6-2.8 mm diam.; pollen exsert-
ed in slender cream-colored threads to 3 mm long.
INFRUCTESCENCES
lipsoid, orange to bright red, 8—11 mm long.

with berries ovoid to subel-

Distribution and habitat. Dieffenbachia crebri-
pistillata is endemic to central and eastern Panama
at (100)250-800(975) m, in Tropical wet forest (Т-
wf), Premontane wet forest (P-wf), and Premontane
rain forest (P-rf) life zones (Holdridge, 1967) in Co-
clé, Colón, Panamá, and San Blas Provinces. While
the species mostly occurs in a few areas of mod-
erately high elevations (including Santa Rita Ridge,
Cerro Bruja, Cerro Jefe, Cerro Campana, and La
Mesa), it dips down to as little as 100 m along the
Colón Province coast in the area of Río Guanche
and Portobelo. Most of these collections differ in
having petioles that dry less orange and have the
petiole sheath ending somewhat below the blade,
never overtopping the blades. As mentioned else-
where under D. nitidipetiolata (and below) these
collections may represent hybrids with either D. ni-
tidipetiolata or D. longispatha.

Phenology. Dieffenbachia crebripistillata flow-
ers principally at the end of the dry season (April
and in the early part of the rainy season from May
to July, less commonly during the balance of the
dry season (January—March) and in the latter part
of the rainy season (August-October). Fruiting time
is poorly known, but most fruiting collections have

—

Discussion. This species is related to D. lon-
gispatha, which differs in being a much more ro-
bust and taller plant (to 3.5 m), having petioles that
dry green and with a long unsheathed portion, and
pistils that are much larger (to 7 mm diam.), many
fewer in number (only to 26), and widely spaced.
See that species for additional discussion of the
differences. Though D. crebripistillata usually has
solid green blades, some plants from Coclé (at La
Mesa near El Valle de Antón and along the Con-
tinental Divide north of Llano Grande) have pale-
maculate leaves. Typically the petiole of Dieffen-
bachia crebripistillata is fully sheathed; however,
some plants from the Cerro Jefe region (Croat
35915, Croat & Zhu 76644, and Dwyer 9497) or
the Río Guanche region (D'Arcy 9678 and Croat
11420) rarely have a significant free portion of the
petiole 3-5(7) em long.

Collections from lowland Colón (Croat 75172,
D'Arcy 9678) are somewhat intermediate between
D. longispatha and the more typical D. crebripistil-
lata from the highlands of Panama. The petioles
are not as fully sheathed, with the free portion of

the petiole ranging from 4 to 5

cm long in these
specimens.

Most collections from El Copé in Coclé Province
have fully sheathed petioles and leaf blades pro-
portionately smaller and narrower, averaging only
25 cm long (vs. an average of 37 cm for all other
populations of the species) and 2.5 times longer
than wide (vs. an average of 1.9 times longer) with
petioles averaging only 11.5 em longer (vs. an av-
erage of 16 cm for other populations). These col-
lections (Antonio 3039; Croat
49155, 67576; Croat & Zhu 76757; Folsom 1265,
3211, 6218; and Sytsma & Andersson 4573) differ
in having smaller elliptic blades. The El Copé re-
gion is well known for having many endemics, and
these plants may represent differences that may ul-
timately prove to be important, but for now are be-
ing considered as D. crebripistillata. One collection
from El Copé in Coclé Province (Croat 74861) dif-
fers from the above only in having the petiole free
above the sheath for a distance of 4.5 cm.

Etymology. The specific epithet is derived from
"creber" (meaning crowded together) and “pistilla
(pistils) and refers to the very closely aggregated
pistils on this species in contrast to the widely sep-
arated pistils of D. longispatha with which the spe-
cies had long been confused.

Paratypes. PANAMA. Coclé: N of El Valle, Cerro
Gaital, Knapp 5758 (MO); El Valle de Antón Region, at
La Mesa, 3.26 mi. above El Valle, Luteyn & Kennedy

Volume 91, Number 4

Croat
Revision of Dieffenbachia

703

1612 (DUKE), FLORPAN, Guerra et al. 5252 (PMA), Lew-
is et al. 1753 (MO), Allen & Alston 1839 (MO); La Mesa,
Fine a ay ade along rd. to Finca Furlong, Croat
CAS, JAUM, M, MO, P, PMA, TEFH,
ca Macarenita, Croat 7478 ae
Divide SW of La Mesa, Stein & Hamilton (MO); I
Mesa, above El Valle de Antón, ca. 2 km W of Cons
Pilón, Croat 37361 (F. MO); above El Valle on be to Cerro
Pilón, krant 25352 (MO); 2 km W of Cerro Pilón, Sullivan
537 (MO); 3 km N of El Valle de Antón, Wilbur et al.
15664 (DUK KE); above El Valle, Croat 13403 (MO); La
Pintada—Coclecito, 5.3 mi. N of stream at л Grande,
gg slope, Croat 49243 (HUA, MEXU, MO, PMA,
jb, VEN); rd. to ig ‘lesito, 12 mi. from us Grande,
Churchill et al. 3993 (MO); past төгү Grande on rd. to
98 (MO); 1

Cascajal. Sytsma et aL 43 Лапо Grande-Cas-
cajal, Hammel 7212 (MO); vic. Alto Calvari 1 №о
El Copé, Folsom 3211 (MO), Folsom 6218 (MO), Folsom

1265 (MO), pepe 3039 (MO); uale El Potroso sawmill,

. Divide. М of El Copé, Sytsma & Andersson 4573
9.4 km ا‎ El Copé, n 44682 (MO),
44558 (МО); Alto Calvario, ca. 4.6 mi. wur El Co
Croat 74861 (MO); Alto Calvario, 5.5 mi. N of El Copé,
3.5 mi. N of Escuela Pb ge Croat 67576 (MO, PMA),
Croat & Zhu 76757 (HUA, К, MO, PMA, TEX),
Croat 49155 (MO, RSA, ЕТ Rio Indio, on rd. from Por-
tobelo to Nombre de Dios, Croat 33568 (MO). Colón: ca.
5 mi. SW of Portobelo, Croat 14175 (MO, PMA); 2 mi. S
of оноро, Croat 11420 (MO); S approach of Cerro Bru-
ja from Río Escandaloso, e 3140 (MO); 9-12 mi
E of Trans-Isthmian Hwy. on Santa Rita ridge, sa
4874 (CM, К, es Santa ni iir 26 km from Trans
Istbmia ian Hwy., Knapp et al. 1717 (MO); Río Gatun, Por-
hints 3820 (MO); E Guanche 3-5
"bride a Croat 26193 (MO), pr» 0678
MO); ca. 3-5 km abovi dod ps 36958 ا‎ ‘a.

(MO "

£

Mc ırtínez
Correa & Montenegro
Correa & Montenegro
ni. from Interamer-

: Sendero del Tigre,
; trail to summit,

‚ Croat 35951 (F,
14707 Mox along trail to summit, Croak
PMA, UB, VEN), Croat 12123 ga pr nee (MO).
Croat pA (MO), C. E. Smith Jr. & H. M. Smith 3389
(F), Luteyn & ей 1 ШШЕ, тк 3761
(МО), Luteyn 3188 (DL ‚ Croat 25213 ; Cerro
Campana, 8.6 mi. SW е; a Luteyn D a
.l mi. above Pan- American Hwy., Croat 74760 (MO);
10 km NE of Altos de Pacora, Mori & Kallunki 6026
(MO); rd. past Altos de Pacora, 3—3.5 mi. NE of Altos de
Pacora, 7.8—8.2 mi. above Pan-Am Hwy., Croat 68699
0.8 mi. e turn-off to Altos de Pacora, Croat
4.6 km beyond peak on rd. to Altos
3 km from Interamerican Hwy., Croat 35915
(MO): Cerro Jefe, Dwyer & Gentry 9479 (DUKE, MO).

7. Dieffenbachia davidsei Croat & Grayum, sp.
nov. TYPE: Costa Rica. Limón: headwaters of
Quebrada Mata de Limón, central fork & hills
betw. central & westernmost forks, Finca Anai

(Sixaola region), 9°35'N, 82°39'W, 25—40 m.

19 Nov. 1984, M. H. Grayum, G. Herrera, A.
Matute & V. Chavarría 4483 (holotype, MO-
3229671*; isotype, INB!). Figures 8. 27B.

Не rba 30-100 em alta; internodia (1.0)1.5—5 cm longa,
5-1.9 em diam.; petiolus 3-11.5 em longus, 5-6 mm
diam. vaginatus 0.4—0.97 longitudinis, pars libera sub-
teres vel D-formata, (1.5)2-5.5 em le om lamina oblongo-
elliptica, 9-26.8 cm longa, 2.3-9 cm lata, nervis primariis
lateralibus (6)9—15 utroque; пуме З рег axillam:
pedunculus 1.5—4 ст longus; spatha 8-16 ст longa; spa-
dix (7.5)10-12.5 ст longus; baccae 8-11 diam.; semina

Slender herb, 30-100 cm tall; sap clear; inter-
nodes (1.0)1.5—5 em long, 1.5-1.9 cm diam., weak-
ly glossy to semiglossy, minutely roughened, usu-
ally with an even mixture of medium vellow-green
and black-green streaks with no obvious back-
eround color, sometimes medium yellow-green to-
ward base with black-green streaks, reversing to
dark black-green with yellow-green streaks toward
the apex, drying obviously minutely wrinkled, stri-
ate and matte. LEAVES spreading-pendent to pen-
dent; petioles 3—11.5 cm long (averaging 6.5 cm
long), 5-6 mm diam., arched-spreading from stem,
sheathed from 0.4 to 0.97 (averaging 0.73) the
length of the petiole, paler than stem, white to yel-
lowish green speckled, especially near the base, the
base often white, tinged with pink and dark-striate;
sheaths auriculate-prolonged at apex (often appear-
ing + acute on dried specimens), the margins in-
rolled on both sides throughout their length, the
opposite sides usually in contact and sometimes in
part overlapping; unsheathed portion (1.5)2—5.5 cm
long, subterete to D-shaped or broadly and obtusely
sulcate, the margins moderately blunt; blades nar-
rowly to broadly oblong-elliptic, 9-26.8 cm long,
2.3—9 cm wide (averaging 20.4 X 5.4 cm), broadest
near the middle, (2)2.7—4.8 times longer than wide
1.9-6.2

times longer than petiole (averaging 3.1 times lon-

(averaging 36 times longer than wide),

ger than petiole), slightly inequilateral, one side 3—
9 mm wider than the other, sometimes weakly fal-
cate, thinly coriaceous, gradually to abruptly long-
acuminate at apex (acumen down-turned and apic-
ulate), acute to rounded or cordulate and nearly
equilateral or markedly inequilateral at base (one
side sometimes also ending lower on the midrib);
margins sometimes undulate; upper surface plain
dark green in Costa Rica, sometimes variegated
with irregular light green blotches in Panama pop-
ulations, glossy to semiglossy; lower surface slightly
paler, matte to weakly glossy; drying dark brown to
dark gray-brown above, yellow-brown to yellow-
green below; midrib flat at base, becoming weakly
toward the concolorous or paler

convex apex,

704 Annals of the
Missouri Botanical Garden

50 mm

-~

Figure 8. Dieffenbachia davidsei. —A. P us «і plant showing habit with several inflorescences. В. Blade adaxial
surface with quilted primary lateral veins. —C. Close-up of stem showing mottled pe tiole and stems. —D. Crown of
plant with cluster of inflorescences, and E showing free-ending sheath apex. —E. Abaxial surface of leaf blade

and immature inflorescence F. Close-up of open more scence

Volume 91, Number 4
2004

Croat 705
Revision of Dieffenbachia

above, convex and paler than surface below, fre-
quently pale-mottled: primary lateral veins (6)9 to
15 per side, flat to sunken, weakly quilted above.
raised and darker than surface below, drying usu-
ally darker than surface below, sometimes. paler
than surface. usually departing midrib at 65-00“
angle throughout most of its length (rarely with the
veins in the distal half of the blade arising at 307—
50°), prominently curved toward the apex in the
outer Y, those near the base to as much as 120°
angle. sometimes forming a weak sigmoid curve,
the primary lateral veins in the upper % to Y some-
times loop-connected for some distance, forming a
weak collective vein 2-5 mm from margin, but this
usually not extending all the way to the apex: in-
terprimary veins almost as prominent as primary
flat to sunken above, weakly raised
INFLORESCEN-

CES usually to 3 per axil. sometimes with more

lateral veins,
and darker than surface below.

than one axil. producing inflorescences: peduncles
4-5 mm diam., ovoid to D-shaped

3.1—4.8

times longer than peduncle, coriaceous, semiglossy

1.54 cm long.
in cross section: spathe 8-16 cm long.
on both surfaces. medium to light green outside.
slightly paler within; tube oblong to somewhat el-
long. oblong-lanceolate when

lipsoid, 6-7 cm

opened, acute at apex (acumen apiculate for 2 mm):

spadix (7.5) 10-12.5 ст long, up to 1.7 em shorter
than the spathe: pistillate portion (4.0)5.5-6 cm
long. (6)8—10 mm wide (the axis ca. 5 mm diam.).

almost contiguous with the staminate portion (:

wide sterile intermediate section lacking): the pis-
tillate flowers more widely spaced near the apex.
1-0 mm apart; pistils 20-35, ovary globose, pale
green; stigma bright yellow with long brushy papil-
lae, 2-2.4 mm diam.;
broadly united at base and forming

staminodia white. usually
an often nearly
complete bowl around the pistil. somewhat flattened
throughout, barely thickened at the apex, 3.1—5 mm
1-0 cm
creamy white, bluntly pointed at apex; synandria

long: staminate portion oblong, long.

irregularly 4- to 6-lobed, drying 1.5-2.3 mm diam..
deeply depressed with the margins turned up. Г\-
FRUCTESCENCES
berries orange, 8-11 mm diam.

with spadix 5.5-7 cm long.
subglobose. 2- to
3-seeded.

Dieffenbachia david-
sel ranges from northeastern Costa Rica to Panama
Pre-

montane wet forest (P-wf), Tropical wet forest (V-wf).

Distribution and habitat.
(Darién Province) and Colombia (Chocó) in

and Premontane rain forest (P-rf) life zones (Hold-
ridge, 1967). In Costa Rica it is known only from
the Sixaola region at 20—40 m elevation. In Panama
it ranges from 100 to 900 m in Panamá Province.

The species frequently occurs in mature forest
along streams.

flowers i

Phenology. Dieffenbachia davidsei

the rainy season sometime after May (one plant
seen with both flower buds and seemingly mature
inflorescences in late October). Mature fruits have
been seen during the dry season, in the late rainy
season, and early dry season from November
through April. Immature fruits have been seen in
late April indicating that flowering may begin even
earlier than May.

Discussion. The species is distinguished by its

slender, dark, semiglossy, mottled stems, mottled

petioles with a prolonged, usually acute sheath
apex, and more or less oblong blades with rather
ne nt primary lateral veins that spread at near-

90°.

Dieffenbachia davidsei is probably most closely

related to D. obscurinervia. That species differs in

usually being a larger plant (to 1.5 m) with prom-
brown internodes, petiole sheaths

inently scurfy

nol

—

which are typically only rounded at the apex
free-ending), and blades which have weakly devel-
oped primary lateral veins that arise at an angle,
usually about 45° to the midrib.

\lthough the broadly spreading primary lateral
veins are one of the most distinctive characteristics
of D. davidsei (with the veins usually spreading
from the midrib at a broad angle even to near the
apex of the blade), a few collections from the El
Llano-Cartí Road in Panama (especially the PMA
sheet of Paredes 940) have primary lateral veins
°. The Paredes 940
collection also has more conspicuously punctate

that spread at angles of up to 45

petioles than does the MO sheet of the same num-
ber. It is possible that Paredes 940 is a hybrid be-
tween D. davidsei and D. obscurinervia. Both spe-
cies occur in the Nusigandí area along the El
Llano-Cartí Road. Dieffenbachia obscurinervia also
has conspicuously mottled petioles, but its veins
The stems of D.
obscurinervia differ markedly in being matte and

arise al a much more acute angle.

scurfv-brown rather than semiglossy. dark black-
green with yellow-green mottling as in D. davidset.
\nother unusual collection, possibly also a hybrid,
is Croat & Zhu 76666 from La Mesa in Coclé Prov-
ince near El Valle de Antón. It has the glossy in-
ternodes of D. davidsei but the veins of D. obscu-
rinervia. |t is perhaps just an unusual collection of
D. obscurinervia.

Etymology. The species was first collected i
Panama by Scott Mori in 1974 along the El L 1
Саг road (Mori et al. 4184). and later in Costa
Hamilton (Dav-

lt is named

Rica by Gerrit Davidse and C. H.
idse & Hamilton 23617) in 1983.

706

Annals of the
Missouri Botanical Garden

honor of Gerrit Davidse of the Missouri Botanical
Garden, co-editor of the Flora Mesoamericana se-
ries.

Paratypes. COSTA RICA. Limón: Quebrada Mata de
Limón, Finca Anai (Sixaola region), Grayum et al. 4440
(CR, MO). PANAMA. Bocas del Toro: Fortuna Lake
Area, Fortuna-Chiriquí Grande, 1.6 mi. N of Cont. Divide,
Croat & Zhu 76533 (MO). Coclé: Cafio Blanco del Norte-
Caño Sucio, Davidse & Hamilton 23617 (MO, PMA); El
Copé, Cont. Divide, Hammel 13685 (MO); El Copé, ca. V
ті. N Lal еар Divide at Alto Calvario, Croat 7,
‚ Hammel 5607 (MO). Darién:
iie Hío Pucuro, vic. Tacarcuna, ca. 18
Puc uro. 10 et al. 16397 (MO). Panamá: El Llano-
3 km from Interam. Hwy., Mori et al. 4184
(MO). San 5 trail to Cerro Camucañala from Río Ti-
tamibe, de Nevers et al. 4709 (MO, PAN); Comarca de
Kunayala, Nusigandf, El Llano—Cartf Rd., 10.1 mi.
Interam. Hwy., Paseo Mariska, Croat & Zhu 77017 (INB,

О); El Llano—Cartf Rd., de Nevers & H. Herrera 3975
(MO); km 18, Galdames et al. 1330 (STRI); Nusigandí, El
Llano—Cartí Rd., betw. Nusigandí pe l mi. N of Nusi-
gandí, Croat & Zhu 76597 (HUA, MO); Sede de Campo
de PEMASKY, ca. 20 km on El Llano—Cartf Rd., Paredes
et al. 940 (MO, STRI); Isla Narganá, бүл, of Rio Dia-
blo, Galdames et al. 1570 (PMA, $ raguas: Cerro
Tute, above Alto de Piedra, = Pherson 10723 (MO).
LOMBIA. Chocó: Nuquí, Ce í, Est. Biol. El Amar-
gal, along trail to Arusf, Croat & Mora 83685 (MO).

~
С
=
=
—
—
М

E
©
=

8. Dieffenbachia fortunensis Croat,

YPE: Panama. Chiriquí: along road between

Fortuna Lake and Chiriquf Grande, 4.5—5 km

N of dam of Fortuna Lake, 8%43'N, 82°17'W,

1100-1135 m, 8 Mar. 1985, T. B. Croat & M.

H. Grayum 60002 (holotype, MO-349012!; iso-
type, PMA!). Figures 9, 28A

sp. nov.

Herba 40-100 cm alta; internodia 1-5 cm longa, 0.8—
2.0 cm diam.; petiolus 12-28 cm кш аы vaginatus 0.37—
0.83 longitudinis; vagina 6.5—14.5 cm longa, decurrens ad
apicem; ae с lance mer raro ШШ anguste
ovata vel a oblanceolata, 15-33 cm longa, 4.5-9.5
cm pta nervis primariis lateralis 0-17 7 3 ; inflo-
rescentia solitaria; pedunculus 4.7-7 em longus; spatha
12-18 cm longa; spadix 9-11.5 cm br

Slender herb, 40—100 cm tall; sap lacking dis-
tinctly foul aroma; stem erect except at base, con-
taining inconspicuous, white raphide cells; inter-
nodes 1-5 cm long, 0.8-2 cm diam.,
semiglossy, dark green to medium green, sometimes
minutely wrinkled and glistening, drying black-
ened, moderately smooth (but minutely granular on
erect-spreading, + clus-

unmarked,

magnification). LEAVES
tered at/near stem apex; petioles 12—28 cm long
(averaging 19.6 cm long), sheathing for 0.37—0.83
their length (averaging 0.58 their length); sheath
6.5-14.5 em long (averaging 10.1 cm), with mar-
gins striate, decurrent distally, dark green, drying

blackened to dark brown, surface matte, striate at

base, minutely granular-roughened throughout with
white raphide cells; unsheathed portion 3-15.5 cm
long, sharply C-shaped, flat-sulcate, with margins
prominently raised; blades narrowly oblong-lance-
olate, rarely sometimes narrowly ovate, or narrowly
oblanceolate, 15—33 cm long, (3.5)4.5-9.5(13) cm
wide (averaging 21 X 6.8 cm) , 2-6.3 times longer
than wide, 0.38—1.48 times longer than petiole (av-
eraging 1.1 times longer), + equilateral or weakly
inequilateral, one side 5-15 mm wider than the
other side, thinly coriaceous to subcoriaceous, dry-
ing papyraceous, usually quilted, weakly bicolo-
rous, + equilaterally or sometimes inequilaterally
acuminate or sometimes acute at apex (acumen
sometimes briefly apiculate), equilateral to slightly
inequilateral and attenuate to acute, rarely rounded
at base; margins usually conspicuously undulate,
drying crisped; upper surface glossy to semiglossy
or weakly glossy, medium to dark green, sometimes
mottled white or cream; lower surface matte to
weakly glossy, moderately paler; midrib flat or flat-
raised and concolorous above, thicker than broad
to convex below, drying brownish matte and darker
than surface to slightly paler than surface, granular-
puberulent to conspicuously granular below; pri-
mary lateral veins 10 to 17 per side, departing mid-
rib at an acute angle, then moderately curved
toward the margin at 55°—90° (mostly 55° in the
middle of the blade but at more acute angles toward
the apex and more obtuse angles toward the base),
turning upward along the margins and forming a
series of fine collective veins along the margins,
some of which extend to the apex, matte, promi-
nently sunken to narrowly or weakly sunken and
concolorous above, thicker than broad or convex
and darker than surface, granular-puberulent to con-
spicuously granular below, drying darker than sur-
face; interprimary veins usually about as conspicu-
ous as primary lateral veins; minor veins moderately
obscure to distinct; “cross-veins” loose-connected,
weakly oblique, drying minutely dark-punctate. IN-
FLORESCENC per axil; peduncle 4.5-7 cm
long: spathe 12-18 cm long, 2-3.7 longer than spa-
dix, 1-1.5 em diam. on tube when furled, gradually
contracted midway, gradually long-tapered to apex,
uniformly pale green on both surfaces; spadix 9—
11.5 em long, drying 3-3.2 mm diam.; free portion
1.5-2 cm long, drying 2 mm diam.; pistillate por-
tion 4.2—6 cm long, drying 7 mm diam. throughout;
fertile staminate portion 5—6.5 cm long, drying

mm diam. throughout; mostly naked intermediate
portion of spadix 1.5-2.0 cm long, drying 2 mm
diam., with a few sterile pistillate flowers in the
lower half; pistils 35 to 38, well-spaced, rarely
more than 2 dispersed across spadix width, de-

Volume 91, Number 4 Croat
2004 Revision of Dieffenbachia

D

11

Figure 9. Dieffenbachia fortunensis. A, B. (Croat 60002). —A. Habit of sterile plant. —B. Leaf blade айах
surface. C—F. (Croat 76340). —C.

xig
Leaf blade abaxial surface. —D. Stem showing petiole bases and free-ending sheath
—EF. Close-up of stem showing acutely and broadly sulcate petiole. —F. Stem showing internodes and petiole bases.

708

Annals of the
Missouri Botanical Garden

pressed-globose, to 1.6 mm long, | mm diam., pale
green; stigma yellow, about as broad as the pistil;
staminodia white, 1—1.4 mm long. conspicuously
thickened, drying pale orange-brown; the synan-
dium 2-2.6 mm long, 1.6-2.0 mm wide, white, dry-
ing yellow-brown, the margins irregularly angular-
subrounded. INFRUCTESCENCE with spadix to 6

em long; berries not seen.

Distribution and habitat. Dieffenbachia fortu-

nensis is apparently endemic Panama, known
only from the Fortuna Dam region of Chiriquí Prov-
ince (hence the epithet) at 900 to 1600 m in Pre-
montane rain forest (P-rf) and Lower montane rain
forest (LM-rf) life zones (Holdridge, 1967)

Phenology. Flowering occurs during the late
dry season and early wet season from March to June
with fruits maturing in the late rainy season after
September.

Discussion. It is distinguished by its usually
small stature, moderately thin, prominently veiny.
undulate, narrowly oblong-lanceolate to narrowly
ovate blades with a flat-raised midrib, and petioles
with the sheath decurrent at its apex and with a
long, free, sharply flattened-sulcate distal portion.
Also characteristic are the granular to granular-pu-
berulent major veins on the lower blade surface.

The species is closest to D. beachiana, the latter
differing having the major veins on the lower
surface conspicuously whitish puberulent and
blades with primary lateral veins more numerous
and spreading consistently at broader angles (most
to са. 90° throughout most of the blade rather than
only a few veins near the base of the blade). In
terms of pubescence D. fortunensis is closer to D.
galdamesiae, which also shares granular puberul-
ence rather than the loose puberulence of D. be-
achiana, but D. galdamesiae differs from D. fortu-
nensis in having the primary lateral veins 15 to 17
per side and arising at a 30°—40° angle (vs. 10 to
17 per side, and at a 55°—90° angle). Dieffenbachia
galdamesiae is also restricted to areas east of the
Panama Canal, while D. fortunensis is restricted to
far western Panama.

The species has been confused with small plants
of D. lutheri, a similar species from Cerro Colorado
in Chiriquf Province. That species usually has wid-
er leaf blades (to 15 em) that are ovate and dry less
blackened. In addition, that species has the pistil-

ate and staminate portions of the spadix contigu-
ous, and lacks the mostly sterile section between
the pistillate and staminate portion as is present on
D. fortunensis.

Paratypes. PANAMA. Bocas del Toro: along Cont.
Divide rd. N off main Fortuna-Chiriquí Grande Hwy.. on

mi. 1.1, Croat & ГА 60346 (МО). Chiriqui: Guala-
ca- С 11 905 Grande, 1S of Cont. Divide & Bocas del
Toro boundary, 1 66866 (MO) 7.2 mi. bevond Los
Planes de Hornito, Croat 67837 (MO); 8.3 mi. NW of Los
Planes de Hornito, Croat 49971 (МО); rd. to Fortuna Dam
i. beyond Río Estí bridge, Croat

18672 (MO, PMA): 4.8 mi. ys vond IRHE facilities at dam,
Croat 68012 (INB, MO, PMA), Croat & Zhu 76340 (MO),
Thompson 4951 (CM, MO); iis Dam are a. Quebrada
os Chorros-Que rada Hondo, to N of reserv £ Chik hill
& Churchill 6158 (MO), ЕП & Chure hill p 59 (MO).

site, N of Gu

9. Dieffenbachia fosteri Croat, sp. TYPE:
Panama. Bocas del Toro: Laguna de Chiriquí,

nov.

Nuri, 15 km E of Punta Cricamola, Ensenada
de Catavela to Quebrada Nuri, 8°55' №,
81 0 N. elevation near sea level, 20 Mar.

1993, R. Foster, A. Herre, E. Kalko & C. Han-
еу 14649 (holotype, PMA!). Figure 27A.

Planta (0.4)1—2 m alta; inte чене) 1.5 em longa, 1.5 en

diam. in sicco: petiolus 10-29 cm longus, vaginatus 4— y
longitudinis, pars libera уйны s gels м a
lanceolata vel anguste ovata, (14)17-28 ст longa.
(6)7-14 em lata, nervis primariis siena 8-13 ut-
roque: inflorescentia 1 per axillam; pedunculus 9.5 cm
longus; spatha 20 ст longa, 2 cm diam.: spadix 18 cm
longus: pars pistillata 6.5 em Mad (in fructu); baccae 6—

7 mm diam in sicco, |-loculares

Slender herb, (0.4)1—2 m tall; sap smelling of
oxalic acid: internodes medium green, dark green-
1.5 em long, drying 1.5 em diam. LEAVES
clustered at/near stem apex; petioles 10-29 cm
long. drying 2-3 mm diam., sheathing % to Y their

mottled,

length; sheath margins drying + hyaline and
brown, sheath apex with one side obscure to round-
ed, with the other side acute; unsheathed portion
of petiole subterete, oval in cross section, 12.5—
18.5 em from base of blade: blades ovate-elliptic to
anceolate or narrowly ovate, (14)1 7-28 X (6)7-14

em. 2-2.4 times longer than wide, somewhat ine-

quilateral, one side 1-1.5 em wider than the other
side, acuminate at apex, the acumen apiculate, 1
mm long, inequilateral and obtuse or rounded at
base: midrib convex to flat-raised and concolorous
above, drying somewhat flattened and concolorous
above, convex and densely hispidulous, darker than
surface below, drying striate with white inclusions
below: primary lateral veins 8 to 13 per side, weak-
ly sunken above, raised beneath, departing midrib
at an acute angle then spreading at 65°—80° in the

lower % of the blade, spreading at 45°-55°

toward
apex, extending almost straight toward the margins
then broadly sweeping toward the apex; upper sur-
face dark green, matte, drying dark brown to some-
what blackened; lower surface slightly paler than
above, weakly glossy, drying slightly less grayish
black than upper surface, densely grayish-speckled

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

below. INFLORESCENCES 1 per axil: peduncle 9.5
em long. 5 mm diam.: spathe 20 cm long. 2 cm

diam., gradually long-tapered, green throughout.
the tube flattening to 3.5 em wide: spadix 18 cm
long, with pistillate portion to 6.5 em long in fruit:

berries 6-7 mm diam., dried, 1-locular.

Distribution and habitat. Dieffenbachia fosteri
is only known from the type in western Panama
near sea level in Bocas del Toro Province in the
Tropical moist forest. (V-mf) life zone (Holdridge.
907).
Phenology. Little is known about the phenology
of this species, but the type collection was in early
fruit in March. Flowering probably occurred some-
time during the rainy season.

Discussion. Dieffenbachia fosteri is character-
ized by its slender, rather weakly sheathed petioles

and especially by its ovate-elliptic. somewhat
blackish-drying blades. It is apparently not closely
related to any other Central American. species,
though in the shape of blades and the decurrent
That

species differs in having semiglossy blades that dry

sheath apex it is most similar to D. killipii.

more or less green. It could possibly be confused
with D. grayumiana, a species ranging along the
Caribbean coast of Costa Rica to western Panama
and probably occurring in the area where D. fosteri
the latter differs from D.
fosteri in having narrowly ovate-subcordate blades

was collected; however,
that are typically conspicuously pale-maculate and
also in drying olive-green to yellowish brown rather
than blackened.

Etymology. The species is named in honor of
one of its collectors, Robin Foster, from the Field
Museum of Natural History in Chicago, an expert
on Neotropical plant ecology and the vegetation of
the Neotropics.

10. Dieffenbachia galdamesiae Croat. sp. nov.
TYPE: Panama. Comarca de San Blas: Pe-
masky, Sendero Nergan Igar. km 15 on El Lla-
no-Carti Road, 9°20'N, 78°58'W, 350 m. 2
July 1994, C. Galdames, T. B. Croat & M. Alla
1222 (holotype, MO-5548504!; isotypes,
AAU!, B!, COL!, F!, GH!, INB!, К!, MEXU!,
NY!, PMA!, RSA!, S!, SCZ!, UB!, US!, VEN!).
Figures 10, 28А.

Planta 50-80 cm alta; internodia 6-20 mm longa. 0.5
2.0(3.0) mm diam.: ei s 18-43
vaginatus 0.25-0.€ ae lamina oblongo- -е Шри-
са, 27-60 cm 1 6.7-18 cm lata, nervis primariis la-
te em 15-17 utroque: ‚юу 'entia 3 per axillam; pe-
dunculus 5.5-15 em longus; spatha 14-25 cm 1 2
em diam.; spadix m longa; pars pistillata 7.

10 cm longa, 8 mm diam.

em longus, C -f ormatus,

Small herb, to 50-80 cm tall: sap lacking foul
odor but weakly caustic to skin: stem supported at
* 0.5-

dark green, weakly to moder-

base by adventitious roots: internodes 6-20
2.0(3.0) mm diam.,
ately glossy; petiole scar oblique. one side 3—4 mm
wider than the other; petioles 18—43 cm long (av-
eraging 29 em long), densely granular-puberulent,
sheathed 0.25-0.66 their length (averaging 0.43
their length); sheath erect to involute, 6.5-20 cm
long (averaging 12.3 cm long).

—

inequilaterally
rounded to acute at apex; unsheathed portion. 10—
ply C-

shaped, broadly concave adaxially: blades oblong-

25 cm long (averaging 16.5 cm long). shar
elliptic, 27-60 ст long. 6.7-18 em wide (averaging

10.8 х 11.7
(averaging 3.6 times longer). 1.1-1.8 times longer

cm). 2.7-4.2 times longer than wide
than. petioles (averaging 1.2 times longer than pet-
ioles). acuminate at apex, acute at base, inequila-
teral, one side to 1.5 em wider than the other, thinly
coriaceous, drying moderately thin: upper surface
dark green and semiglossy, drying dark brown to

olive-green: lower surface slightly paler, almost
matte, drying weakly glossy, grayish to yellowish
brown: midrib broadly convex-flattened and con-

darker

drying

colorous above, narrowly rounded, matte,

and sparsely granular-puberulent below,
darker than surface, flattened to ridged with one or
both margins narrowly raised; primary lateral veins
15 to 17 per side, arising at 30°—40° angle, sweep-
ing prominently toward the apex with as many as
4 to 5 of them simultaneously coursing along the
margin within | em of the margin, sometimes form-
ing weak collective veins, weakly quilted-sunken
above. convex and sparsely granular-puberulent
and somewhat scurfy below, drying darker than sur-
face with the center collapsed and the margins of-
ten thin and upturned; minor veins obscurely to
moderately visible and darker than surface above.
cross-veins sometimes
INFLORES-
CENCES to 3 per axil; peduncle 5.5-15 em long.

drying moderately distinct:

drying moderately distinet below.

5-8 mm diam., drying 2.5-5 mm diam.: spathe 14—
25 cm long, 1.6-2.5 times longer than peduncle, 2
em diam. at tube, green on both surfaces: spadix
15.7-18

tillate portion of spadix 7.3-10 em long. 8 mm

em long: free portion 9.5-12 em long: pis-
diam.: staminate portion of spadix 7-8.5 cm long.
6 mm d pu :
1.3-2

the Y: pistils 59 to 68, moderately closely

the mostly sterile intermediate portion
.5 em long with a few pistillodes extending in

spaced, 2 to 4 situated across the width of the pis-
tils: 1.2-2.0 mm diam.:
diam., depressed-globose; staminodia club-shaped,
1.8-2.8 mm long, 0.4-1.0 mm wide, flattened, free
to base, not expanded toward the base. thickened

ovaries stigmas 1.6-2.2

710

Annals of the
Missouri Botanical Garden

of stem showing roots and petiole bases. —D.

and somewhat granular-puberulent at apex; syn-
andria 2.4-2.8 mm diam., irregularly rounded,
broadly sulcate to truncate with slightly overlapping
edges, the margins + crenulate. INFRUCTES-
CENCES not seen.

Distribution and habitat. Dieffenbachia galda-
mesiae is endemic to Panama, known only from
central Panama on both sides of the isthmus in the
Tropical wet forest (T-wf) life zone (Holdridge, 1967
at 350 to 500 m elevation. It occurs in swampy
conditions in creek beds in virgin forest in nearly

full shade.

Figure 10. Dieffenbachia galdamesiae (Croat 76560). —
i ). Petioles and clusters of inflorescences.

~

Ty"
р

A. Habit. —B. Leaf blade adaxial surface. —C. Close-up

Phenology. The species has been seen in flow-
er in June as well as in October. Mature fruits have
been seen in December.

Discussion. The species is characterized by its
moderately small habit, only to 80 cm tall, the gran-
ular-puberulent petioles and major veins on the
lower blade surface. It is most closely related to D.
beachiana and D. fortunensis, differing from both
in having the primary lateral veins ascending at
less than a 50* angle. It may prove to be only sub-
specifically distinct from D. fortunensis.

Etymology. The species is named in honor of

Volume 91, Number 4
2004

Croat 711
Revision of Dieffenbachia

Chilean botanist Carmen Galdames, a long-time
resident of Panama, who has collected in Panama
for the SCZ herbarium at the Smithsonian Tropical
Research Institute. Carmen was the first to bring
the species to my attention and also collected the
type specimen.
Paratypes. PANAMA. Panama: El Llano-Cartí Rd.

6.8 mi. from hwy., Croat 49124 (MO). San Blas: Comarca
de Kunavala, Nusigandí, E 1 Llano artí Rd.,

Trail).

9 mi. N of

Croat * Zhu

eborita, 16-17 km NW of Santa Fe, Dressler 5316 (MO).

11. Dieffenbachia grayumiana Croat, Novon 9:
494. 1999. TYPE: Costa Rica. Limón: Refugio
Nacional Barra del Colorado, forests and pas-
tures between. Río Chirripócito and. Río Sar-
dina [Sardinal], 10%8N, 8375'W, 12 m. М. H.
Grayum 9773 (holotype, MO-4370212!;
type, INB!). Figures 11, 27А.

iso-

Stout herb, 1-1.5 m tall; stems erect at apical
part, the older portion reclining for up to 1.5 m;
internodes 2.5-8.5 em long, 2—3.5(—10) ст diam..
dark green. glossy, variegated with cream-yellow or

к”

pale green (sometimes medium green with dar
green lines as in Croat & Grayum 60149); petioles
(24—)30—59 39 long).
sheathed from 0.3 to 0.55 their length (averaging
0.42).
streaked or tinged with cream-white in lower half,
especially near the base, subterete: sheath 19—29
em long, usually decurrent at apex,

em long (averaging em

matte, dark olive-green to deep brown,

sometimes
weakly free-ending (as in Croat & Grayum 60149):
unsheathed portion 13-28.5 cm long. weakly sul-
cate adaxially, weakly flattened toward the apex.
sometimes slightly white adaxially and continuing
white onto lower midrib; blades narrowly ovate to
oblong-ovate, (22)30—54 X 10-32 cm (averaging
36 X 18 em), 1.5-2.6 times longer than wide (av-
eraging 1.9). ranging from 0.6 as long as petioles
t
about as long as petioles, slightly inequilateral, one
side 1-1.5 em wider than the other,

=

› 1.4 times longer than petioles, but averaging

acuminate to
abruptly acuminate at apex, inequilaterally subcor-
date (sinus to 3.5 em deep) or rarely inequilaterally
rounded at base (sometimes one side weakly sub-
subcoriaceous,

cordate, the other side rounded),

drying thin, slightly concolorous to slightly bicolo-

rous; upper surface usually glossy to semiglossy.

dark green, to weakly mottled cream, drying dark
plain (unvariegated) to usually con-
spicuously mottled vellow-cream: lower surface se-

olive-green,

miglossy to nearly matte, slightly paler, drying yel-
lowish green; midrib flat to weakly flat-raised or
broadly convex (sometimes broadly sunken at base,

broadly flat-raised and striate toward apex) slightly
paler and dark green-spotted to concolorous above,
convex to narrowly rounded and white or narrowly
acute and paler below; primary lateral veins 13 to
18(to 22) per side, gradually arising at a steep angle
from the midrib, then spreading in a broad curve
at 5580” angle, (those near the apex to 25° angle.
those near he base sometimes 907—110? angle and
sometimes forming a sigmoid curve). deeply sunken
above, convex below, forming a series of weakly
developed collective veins that eventually merge
with the margin; at least the midrib and primary
lateral veins sometimes minutely farinose-granular:
minor veins moderately obscure below. INFLO-
RESCENCE I to 3 per axil, sometimes subtended
by a reduced leaf with a fully sheathed petiole (the
sheath ше at apex) and a reduced leaf
blade, 12- 3.5—6.5 cm: 7 lies 8-12 cm
long, drying 2934 mm diam.; spathe 16.5-23.5 cm
long. 3—4 em longer than the spadix, 4.0-5.0 ст
wide at base, to 2.5-3.5 em wide at constriction,
2.5-3 cm wide on blade (to 7 em wide when flat-
tened). uniformly light green to medium green on
both surfaces, weakly glossy throughout outside,
somewhat glossier within; spadix 15-27 cm long:
free portion 7-13 cm long: pistillate portion 8.0—
9.3 ст long. drying 7—10 mm wide; staminate por-
tion 5—6.5 em long, white, tapered toward apex and
tapered slightly toward the base: the staminate and
pistillate portions separated by an almost sterile in-
termediate segment 2-2.5 cm long with a few scat-
tered pistils in the lower half and a few scattered
to 160, dense-
ly aggregated, separated from one another by 0.5
to 2.5 times their width, irregularly scattered with

staminodia in upper half; pistils 115

roughly 4 to 5 covering the width of the spadix:
ovaries pale lemon-yellow, depressed-globose, 1.8—
2 mm wide; staminodia white, 3 to 5 per pistil, free
or briefly united at base, 1.5-2.2 mm long: synan-
dria 1.2-1.6 mm diam.. irregularly angled with
rounded margins. INFRUCTESCENCES to 27 cm
long. with fruiting portion 10-14 cm long; berries

red-orange, subglobose, ovoid to ellipsoid, 5-7 mm
diam.

Distribution and habitat. Dieffenbachia grayu-
miana ranges along the Atlantic slope from north-
western Costa Rica to western Panama, mostly near
sea level but ranging up to 1300 m in Costa Rica
in Alajuela Province (vic. of Monteverde Reserve)
and to 480 m in Heredia Province. Grayum (pers.
comm.) reports the species to occur mostly in light
gaps and disturbed areas in primary forest at the
La Selva Reserve in Costa Rica.

Phenology.

Flowering occurs in D. grayumiana

Annals of the
Missouri Botanical Garden

D

Figure S Dieffe em grayumtana. —A. Habit (Croat 60149). B-D. (Croat 74953). —B. Leaf blade adaxial
surface. —€. Blade abaxial surface. —D. Apex of stem showing heavily sheathed petioles with sharply sulcate free
Porton, me а petiole bases.

Volume 91, Number 4
2004

Croat 713
Revision of Dieffenbachia

from January to June, rarely as early as November.

Fruiting collections have been seen only from May
to September.

Discussion. Тһе species is characterized by its
narrowly ovate, typically subcordate, mottled
blades: weakly sheathed, decurrent petioles; and
variegated stems and petioles. Also characteristic
are blades that are frequently glossy on the upper
surface and matte or nearly so on the lower surface.
The major veins are sometimes minutely farinose-
eranular on the lower surface. In this regard it is
similar to D. beachiana, a species with puberulent
major veins on the lower blade surface. Aside from
pubescence type, D. beachiana also differs in hav-
ing much narrower blades (1.8-5.3 times longer
than wide) with more numerous pairs of primary
lateral veins (23 to 36 pairs).

Dieffenbachia grayumiana is superficially simi-
lar to D. seguine from the West Indies in the shape
and coloration of its dried blades but lacks the
sharply sulcate petioles, the bicarpellate ovaries,
and the protruding stubby spadix with a reflexed
spathe blade seen in the latter.

Toro Province it
Panama (Croat 74945) differs in having larger con-
colorous blades (54 X 30 em) that are only weakly
glossy on the upper surface, with only weakly sunk-

A collection from Bocas del

=

en primary lateral veins. Another collection from
Bocas del Toro, Croat & Grayum 60149, had stems
lo ca.

10 cm diam., substantially larger than those

of any other collection reported.

Additional s] examined, COSTA RICA. Alajue-
la: Puntarenas- ези aste, Рейаѕ 5 e Dryer 1681 (V):
Rio Peñas Blancas, Burger et al. 10734 (CR, К); Upala, Río
Zapote, 5 km S of Canalete, Burger & 9 7 5 9968 (CR, F).
Río Sapio, La Virgen. 1974. Horich s.n. (M):
Hío Peje- Río Guacimo,
2 3 (D U КЕ Secondino’s woods, off (
Kress 64-1632 (SEL); Río Peje 17 5
of cat Barva, T 66867 (MO); San
vic. of Chilamante, 11.6 mi.
(B. CR, M, MO); La Selva, Croat 78733 (COL, IN
SEL); ee on Rio Puerto Viejo, е & Matta
1181 (CR, F); OTS Field Station along Río Puerto Viejo
just E. of jet. a Río Sarapiquí. Beach wes (DUKE).
Beach 1441 (DUKE), 10 207 (DUKE). Croat 44321
(МО), 7 0 9724 s Ватт. 600 Hammel
3473 KE), m ui (DUKE). Limón: Ref. Gan-
doca- Manni Río Gandocaca, usus et al. 8038 (CR,
air km S of Islas Buena Vista in the Río Colorado,

16 La sw of Barra del Colorado, Davidse & Herrera 31213
(INB, MO); Cerro о E of Janto, Sleveris
| ат 5 55 MEXU, : Río Срб ito-Hío Sardina,
Barra del С ed Río Chirripócito- Hío Sardina,
9830 (MO); Guac Mee Rd., Barringer
; B. lac. Tortuguero, Río Suerte betw.
año Penitencia, Gann et al. 11116 (INB.
MO): Lomas de Sierpe, 8 from Rio Tortuguero, Grayum et

al. 11163 (INB, MO). PANAMA. Boeas del Toro: Almi-

rante-Bocas del Toro, near Milla 5, Croat & Porter 16499

MO): Chiriquí Grande-Fortuna, 3 of Chiriquí
Grande, Croat & тит 00149 (М. мо, PMA, US): Gual-
aca-Chiriquí Grande, 8.1 mi. S of Punta Peña, Croat 7 74953

(MO, PMA). Chiriquí: Lae ne Grande, 1.4 mi. S
of Punta Peña. Croat 74945 (MO). M. Akers 784 (MO).

12. Dieffenbachia e soe Croat & Grayum,
Novon 9: 496. TYPE: Costa Rica. He-
redia: Finca La iim O.T.S. Field Station on
the Río Sarapiquí, 50-80 m. M. H. Grayum
7670 (holotype, MO-3491533!; isotypes, B!.
CR!, K!). Figures 12, 27B.

Small herb. 25—40(70) em tall; sap not foul-

smelling; stem becoming decumbent and subrhi-

zomatous at base; internodes 1-1.5(2.7) em long,

on lower portions, 3.5—7.5 cm long toward the apex.

—

5-2 em diam., glossy, dark blackish green, drying
striate.
725035) cm long
(averaging 15 cm long), erect, green or mottled with
dull

yellowish brown,

yellowish brown to gray-green, weakly

LEAVES erect-arching; petioles
yellow-green, drying greenish to sometimes
surface drying matte, sheathing
for (0.3)0.1—0.8 the petiole length (averaging 0.63
their length), sheath 5.5-13 cm long (averaging 8
em): unsheathed portion 1-9 ст long, rarely to 15
em long. narrowly C-shaped to D-shaped in cross
section, narrowly sulcate adaxially, with margins
finely acute, the tip narrowly decurrent, sometimes
blades
г oblanceolate, 9-28
x 7.5 cm),

times longer than wide (averaging 2.7

difficult to discern where it ends: narrowly
3.2-
1.7-3.4

times

broadly elliptic o
13(15) cm (averaging 19.5
longer
than wide), 1.1-1.5 times longer than the petiole;
equilateral to slightly inequilateral, one side 0.5-1
em wider than the other (the narrower side usually
plane, the wider side usually minutely undulate).
weakly to semiglossy, acuminate, narrowly to broad-
ly acute or attenuate at apex, and equilateral «
slightly inequilateral, rarely obtuse at base. thinly
coriaceous, slightly to moderately bicolorous: upper
surface medium to dark green, weakly glossy to se-
miglossy. drying light yellow-green to dark brown:
lower surface weakly glossy to matte. slightly to
moderately paler, drying yellow-green, sometimes
midrib flat-raised, convex

vellow-brown: rarely

(sometimes obscurely sulcate medially), 1-3 mm
diam., slightly paler than surface above. convex to
narrowly convex below, drying pale brown. matte.
with short, white raphide cells: primary lateral veins
9 to 17 per side, departing midrib at a 40°—50°
angle. weakly curved to the margins, weakly sunk-
en or slightly raised in weak valleys. weakly quilted
and concolorous above, convex and weakly pleated-
raised, drying moderately

inconspicuous, slightly

Annals of the
Missouri Botanical Garden

Qu E

E. (Croat 78758). —A. Habit of pl int in the wild. T Potted flower ring

‘igure 12. Dieffenbachia ا‎ \,
d showing habit (Duke 81-1 —C. Potted plant Ego inflorescence at anthesis (Croat 78731). D. F. (Croat 787.
—D. Leaf bases and 9 0 85 of йе, 'scences, the one on the right at ап! Ee E. Crown | plani n an open
inflorescence. —F. Crown of plant with a cluster of ре 'scences (one eut away to expose full-sized berries

Volume 91, Number 4
2004

Croat 715
Revision of Dieffenbachia

darker than surface or slightly paler than surface
below; the interprimary veins almost as conspicu-
ous as primary lateral veins; minor veins darker
than surface below, drying moderately faint; “cross-
veins” darker than surface below, drying moderate-
ly faint. INFLORESCENCES 1 to 3 per axil: pe-
duncle 4.5-11 cm long, subterete in cross section:
spathe (8) 10-16 em long, 1.3-2.7
peduncle, medium green throughout, and weakly

times longer than

glossy outside, medium green and glossy inside,
cuspidate to acuminate at apex: spathe tube 6.5—
1.2-2.3 cm diam., free portion 3-6
em wide when flattened; spadix 6.5-15.5 cm long;

12.5 cm long,

free portion 4.7—7.5 cm long; pistillate portion 5—
8.5 em long. 6—7 mm diam. throughout, fused with
spathe for up to 4 em: fertile staminate portion ta-
pered to both ends. moderately acute at apex.
(1.7)3—4.5 em long, 6—7 mm diam. throughout; ster-
ile intermediate segment (0.8)2—3 cm long. with a
few scattered staminodia throughout; pistils 26 to
43, ovoid, sparse to moderately dense, loosely scat-
tered in clusters of 2 to 4 with up to 3 across the
width of spadix but often with spaces between the
groups of pistils up to twice the width of the spadix,
sometimes in a spiral with up to 5 to 6 pistils: ova-
ries 1-locular, 2.4 mm long, 2.4 mm diam.; stigmas
1.6-1.8 mm diam.: staminodia 2.8—3 mm long, up
to twice as long as pistils, free from one another at
base. thickened at both ends, white at apex, but
often translucent midway and drying flattened and
very thin: synandrium bluntly 4- to 5-sided, mar-
gins irregularly shaped toward the base, + rounded
at apex, 2-2.5 mm diam. INFRUCTESCENCE with
spathe pale orange outside; spadix 22 cm long; ber-
ries orange to bright red, obovoid-ellipsoid, 1 cm
long, 8 mm diam.

Dieffenbachia ham-
melii occurs in southeastern Nicaragua (Dpto. Río

Distribution and habitat.

San Juan) and northern Costa Rica from sea level
to LOO m in the Tropical wet forest (T-wf) life zone
(Holdridge, 1967), in wet forests and swampy areas
on the Atlantic slope.

Phenology.
have been seen from March through May and also

Flowering plants of D. hammelii

July, while mature fruits have been seen in August
and September. Cultivated plants at the Missouri
Botanical Garden flowered in mid July and mid Oc-
tober.
Discussion. The species is characterized by its
small stature, typically 25-40 cm; its glossy, de-
cumbent, subrhizomatous stems; weakly sheathed,
matte-drying petioles (sheath decurrent at apex):
and moderately small, more or less oblong-elliptic.
weakly inequilateral green leaf blades with mod-

erately numerous primary lateral veins. One blade
margin is usually plane and one margin usually mi-
nutely undulate.

In Costa Rica it is most easily confused with D.
oerstedii or small plants of D. grayumiana, both of
which can be distinguished in having the petiolar
sheath auriculate at the apex rather than decurrent
as in D. hammelii. At La Selva, where the species
was first studied, One
collection (Hammel 8784) reported that the sap was
not foul smelling, as is the case with many species.

D. hammelii is uncommon.

Additional specimens seen. COSTA RICA. Heredia:
Finca La Selva, OTS Field Station on the Río Puerto Vie-
jo. Grayum 2772 (DUKE, MO). Limón: inte up near
Boca de 185 Lagunas de Tortuguero, Burger & Antonio
11224 (CR, F); Cerro Coronel, E of Rio Pa at km from
d rus of v Colorado, Stevens 24257 (CR, MO); 2 air km

SSE of Islas Buena Vista in the Río € irme: Davidse &
Herrera 31077 (CR, MO); 3.5 air km S Islas Buena
Vista in the Río Colorado, Davidse & odis 31154 (MO);
Hef. Barra del ied big ts Grayum et al. 9744
(CR. MO): Pococi, Tortu », N end of Lomas de Sie rpe.
S from Río EN sun et al. 11169 (CR. INB,
MO). San uez de Coronado, Braulio Carrillo
NP. along San José to Siquirres Hwy., along D to. Río
Sucio, Old Carillo 7 7 td Croat 78758 (COL, СОЕТ,
INB. MEXU, MO, PMA,’ „UB. WU). NIC "i AGUA.
Rio San Juan: near Cafio rete no, 20 km NE of El
Castillo, Neill & Vincelli 3484 (MO); “Marcelo” near Río
Salick 8092 (MO).

José: Vaz

Sabalos,

13. Dieffenbachia horichii Croat & Grayum, sp.
nov. TYPE: Costa Rica. San José: Cantón Pérez
Zeledon, along road betw. San Isidro General—
Dominical, Fil: Tinamastes, 9?18'24"N,
83746' . 900-1100 m. T B. Croat & D.
Hannon 79115 holotype. MO- es iso-

s, AAU!, B!, CAS!, COL!, CRL DUKE!, F!,

GH!, HUA!, INB!, K!, MEXU!, NY!, P!, PMA!,

QCNE!, RSA!, S!, SCZ!, TEFH!, TEX!, UB!,

US!, VEN!, WU!). Figures 13, 27A.

Planta terrestris, 1.0—1.5(2) m; internodia 1-3 cm lon-
ga, 4—6 cm diam.; petiolus 833. cm longus, vaginatus fere
omnino; vagina libera 1.5 cm bun lamina elliptic a vel
ovato-elliptica, 26-60 em longa, 9—30 cm lata, nervis pri-

mariis lateralibus 14—21 poque. inflorescentia 3-6 in
quoque axilla; pedunculus 8.5-19 cm longus; spatha
14.5-32.5 em longa; spadix 13- TP cm longus; pistilla 43—
09

Stout herb, 1—1.5(2) m tall; sap white, copious,
foetid, caustic; stem erect on younger parts, to 1.2
m long and reclining on older parts, internodes 1—
3 cm long, 4—6 cm diam., semiglossy to glossy, dark
green to medium green; petioles 8-33 cm long (av-
eraging 18.7 em long), weakly glossy, sheathing
nearly or completely throughout; sheath. medium
green streaked with yellow-green, margins involute,
the tip free-ending and inequilaterally rounded-au-

716

Annals of the

Missouri Botanical Garden

Figure 13. Dieffenbachia horichii. A, B.
plant with cluster of inflorescences. C, 5 E. (Croat 7907.

of stem with petiole bases. —E.

riculate (auricle sometimes extending up to 1.5 cm
beyond blade): unsheathed portion lacking or to 1.2
em long (rarely to 6 em long). obtusely somewhat
flattened in cross section: blades narrowly to broad-
x 9-30 cm (av-
1.9-3.4 times longer than

ly e Прие | to ovate-elliptic, 20-60 х
eraging cm),
wide 5 2.5 times longer), 1.7—4 times lon-
ger than petiole, slightly inequilateral. опе side
0.5-1.2 em wider than the other side, subcoria-

ceous to coriaceous. somewhat bicolorous. acumi-

(Croat & Hannon ЕИ —

3).

mm

9mm
Ld

E

\. Habit of flowering plant.
. Plant with inflorescence at anthesis. . Clos

= Crown of
Close-up

C лө of lamina base and с be -up of inflorescence.

nate at apex, + equilateral and obtuse to rounded

(rarely acute or narrowly rounded) at base, margins
weakly undulate; upper surface dark green, semi-

glossy to highly glossy, drying dark gray-green to

dark yellow-brown: lower surface weakly glossy to

matte, moderately paler, drying yellow-brown to

yellowish green; midrib broadly and shallowly

sunken to flat-sunken above, 5-20 mm diam.. con-

vex and bluntly low-triangular below, drying light

brown to dark brown paler than surface below: pri-

Volume 91, Number 4
2004

Croat 717
Revision of Dieffenbachia

mary lateral veins 14 to 21 per side, departing mid-
rib at a mostly 307—40* angle above middle, often
70°—90°, often arising at an acute angle, spreading
to the margins. broadly curved toward apex. even-
tually merging at margins, weakly sunken above,
weakly convex below, drying brownish and darker
than surface below: the interprimary veins usually
darker than surface, 1 between each pair of primary

ateral veins: minor veins visible, slightly darker
than surface, drying moderately obscure on lower
surface. INFLORESCENCES 3 to 6 per axil: pe-
duncle 8.5-19 cm long (averaging 13.5 em). 3-6
mm diam., drying striate; spathe 14.5-32.5 cm
long. 4—5.5 cm diam. (averaging 20.8 cm long).
2.54 cm diam. at constriction, 0.9-2.3 times lon-
ger than the peduncle (averaging 1.5 times longer
than the peduncle), gradually long-tapered toward
apex from midway, light green to medium green
throughout; spathe tube 3 X 2.3 em diam. when
furled (flattening 4.0—5.5 em wide), the constricted
area flattening 2.5—4.0 em wide: spathe blade 2.5—
4 cm wide at anthesis; spadix 13-27 em long (av-
eraging 17.4 cm long); free portion 10-13.5 cm
long: pistillate portion to (6.5)8-10.8 em long (av-
eraging 8.3 cm long), 8-17 mm wide. drying 8 mm
diam.; fertile staminate portion 8.3-12 ст long.
cream-colored, moderately tapered toward apex and
weakly tapered toward base, 7-12 mm diam. mid-
way: mostly sterile intermediate segment 1.7—3.7
em long, with a few scattered staminodia through-
out: pistils 43 to 69, irregularly scattered. nearly
contiguous, 3 to 4(6 to 7) dispersed across spadix
width, separated from one another by up to 4 times
their width; ovary depressed-globose. 2 mm long.
yellow-green; stigma cushion-shaped, 2.8-3.4 mm
diam.. about twice as wide as thick and usually
broader than the pistil at anthesis. yellowish: sta-
minodia white, 3 to 5 per pistil. 3—1 mm long. free
or briefly united at base: synandria 1.6-3.0 mm
diam., subrounded, depressed medially at apex.
drying orange-brown. INFRUCTESCENCE 19-24
em long: spathe orange outside: spadix 8-15 em
long; berries red. subglobose, ovoid to ellipsoid, 7—
10 mm long.

Distribution and habitat. Dieffenbachia horichii
is known only from the Pacific slope of Costa Rica
from the Carara reserve and Puriscal region to the
San Isidro region and Dominical. It occurs in Pre-
montane rain forest (P-rf) and transition forests be-
tween Tropical wet forest (T-wf) and Premontane
rain forest (P-rf) life zones (Holdridge. 1967).
sea level to 900 m.

Phenology. Dieffenbachia horichii begins to
flower in the early rainy season from May to July.

from

but flowering collections have also been seen in
September. Immature inflorescences have been
seen from November to May, and mature fruits have
been seen from the late rainy season (November

—

to early rainy season (late June).
Discussion. The species is characterized by its
fully sheathed petioles, involute petiolar sheath,
and by its thick and more or less elliptic, semi-
glossy to glossy, mostly unvariegated blades that
dry somewhat greenish to yellow-brown.
Dieffenbachia horichii is closely related to two

other species with petioles fully sheathed or nearly

—

These are D. panamensis and D. standleyi. In
comparison with D. horichii,

similarly shaped blades and petioles fully sheathed,

D. panamensis has

but that species differs in having the petiole sheath
usually flaring and recurled rather than involute as
in D. horichit. It also has leaf blades with the upper
surface matte and subvelvety that dry blackened.
Another difference is that H. panamensis occurs
principally on the Atlantic slope of central Panama,
whereas D. horichii occurs on the Pacific slope of
Costa Rica

Dieffenbachia horichii is likely to be confused
with D.

mostly winged petioles. That species occurs on the

standleyi, another species with fully or
Atlantic slope of Honduras and Nicaragua, and dif-
fers by having the petiole sheath erect and recurled
outward along the margins and acute at the apex
with the sheath margins markedly undulate (vs. the
sheath margins involute and smooth). The petioles
of D. standleyi are also longer on average, frequent-
ly more than 25 cm long, and average 30 em long
(vs. frequently less than 25 em long, averaging less
than 20 cm long for D. horichii). In addition, the
upper midrib on the blades of D. standleyi is broad-
ly concave, whereas on D. horichii the midrib is
broadly convex with a medial sulcus but with the
entire midrib sunken in a valley.

Most of the typical material of D. standleyi has
been collected in the Lancetilla Valley and its vi-
cinity in. Honduras, and has blades considerably
longer on average than those of D. horichii. Some
collections in Nicaragua and in western Costa Rica
are unusual. Stevens 7457 from Zelaya and Moreno
17142 from Matagalpa dry a darker yellow-brown.
The only other species in Central America that has
a fully sheathed petiole is D. tonduzii. Dieffenbach-
ta tonduzit is distinguished by having smaller and
thinner blades (rarely to 45 cm long and 20 cm
wide) that are usually matte to weakly glossy above
(vs. usually glossy in D. horichii) with more primary
lateral veins (18 to 25 vs. usually fewer than 20 in
D. horichii). Grayum 4757, from the Carara Re-

serve in Puntarenas Province, is perhaps a hybrid

718

Annals of the
Missouri Botanical Garden

between D. horichii (Grayum 4756) and D. oerstedii
(Grayum 4765). It differs in having petioles that are
narrower and less fully sheathed.

Etymology. The species is named in honor of
horticulturist Clarence Horich, who made the first
collection of the species.

Paratypes. COSTA RICA. Puntarenas: San José
Province, Playa Dominical-San Isidro del General Baru,
1155 8 Burger et al. 10669 (F, MO), Burger & Baker

10137 (C p» а а Bonita, Сагага Res., Gra-
yum et FI 57 (IN В, ‘inca El Edén, km 183, К.
OO m » of Santa ы, rta, бте: 22951 (B. CM

CR. 0 Quebrada Bonita, ( ‚ Grayum 4756
(CR, MO), Croat 79073 (КАР, INB, MO. PMA); hills at
SW part of Montañas Jamaica, ca. 2.5 km NE У 92 10
de Turrubares, Carara Res., Grayum et al. 54 MO
San José: Par. Nac. Braulio Carrillo, Quel аи
tue Ча, Chavarría & Umaña 157 (С О); Zona Prot. La
Cangreja, vic. Quebrada Grande, ca. 2 km NNE of Mas-
m de rii al, Grayum 8638 (CR, MO); ZP La Cangre-
of Santa Rosa de Purisc al, Grayum et al.

Q
~

=
a

>
м

Quebrada Bonita, Chacón 1406 (CR); C ordille га Talamai
ca, Río He 'rmoso, xs inca El Quizarra, IL. Williams et al.
28479 (F, NY, Acosta, along Río Parritilla, ca. 1 km
E of Zoncuano, о. et al. 11174 (INB, MO); Pérez
Le ledón, Fila n Valverde 741 (CR, MO); Puriscal,

ila Túfares, Salitrales de Puriscal, Gómez-Laurito 7792
(CR); Z.P. La Cangreja, с erros de Puriscal, San Martin de
Puriseal, La Fila Vara Blanca, J. Morales 2035 (CR, INB,
MO).

Cultivated specimens. Costa Rica. 800-900 m, culti-
vated at Munich as 1203/74, Horich s.n. (M).
14. Dieffenbachia isthmia Croat, sp. nov.

l'YPE: Panama: along trail betw. Río Maje &
Quebrada Brava, 60 m, 4 May 1976, T. B.
Croat 34656 (holotype, MO-240198*; isotypes,
В!, K!, PMA!, US!). Figures 14, 28A

Planta 5 ad | m; internodia 0.5-3 em longa,
2-3(4.5) em diam., atroviridia; petiolus ! 1-34( 10) em lon-
gus, a 0.4—0.77 longitudinis, vagina 8. e cm
longa: lamina oblongo-ovata vel anguste ovata, (12)15—
30(39) cm longa, (6)10-26 cm lata, plerumque ene
data, nervis npe lateralibus 7—12(15) utroque: inflo-

r quoque axillam; pedunculus (2.5)4—
5 cm oia spatha 15-17.5(23) em longa, apadix
10.5-15.8 em longus; pars feminea 6.5-9.5 cm longa, 1.4
em diam.; pars masculina 6-7.5 cm longa.

—
ta
a

rescentia 3-5

Medium-sized herb, usually to no more than

m tall (rarely to 1.5 m tall); sap watery, sometimes
white; stem creeping over surface of ground at base,
then erect; internodes weakly glossy, 0.5-3 cm long.
2-3(4.5) em diam., dark green, drying dark yellow-
LEAVES scat-
tered along stem, denser near apex; petioles 11-
34(40) cm long, (averaging 26 cm long), moderately
soft, sheathing to midway or slightly above, for 0.4—
length):

brown, olive-brown to blackened.

0.77 their length (averaging 0.55 their

sheath 8.5-21 cm long (averaging 14 cm), with
margins drying thin, light brown and minutely un-
dulate, the tip inequilaterally acute to emarginate
and free-ending; unsheathed portion flattened or
rounded and becoming weakly sulcate toward apex
in cross section (never sharply sulcate), blunt to
moderately acute, rarely broadly and bluntly sul-
cate; blades oblong-ovate to narrowly ovate, (12)15—
30(39) cm long. (6)10-26 em wide (averaging 26
х 16 cm), 0.78-1.77 times longer than petiole (av-
eraging 1.1 times longer), inequilateral, one side
0.5-2.6 cm wider than the other side, thinly cori-
aceous, abruptly to gradually acuminate at apex,
acute to cordate at base, the sides often + unequal,
usually subcordate with at least one side subcor-
date at base; upper surface matte to weakly glossy,
dark green, drying dark gray-green to sometimes
blackened; lower surface matte, paler, drying yel-
lowish gray-brown to dark yellow-brown; midrib 5—
flat to broadly and obscurely sunken
at base, weakly raised toward apex above, conco-
lorous to slightly paler than surface, frequently
much paler than surface or even white toward apex,
often with a light green streak distally, drying paler
than surface or darker than surface above, convex

8 mm diam.,

to bluntly round-raised, drying somewhat flattened
with acute ribs below, drying darker than surface
to 12(15) per side,
departing midrib at a 455559 angle (to 30°—50° at
apex, 50°-90° at then
spreading weakly or not at all sunken, often green-

below: primary lateral veins 7

base), arising acutely,
ish toward apex, sometimes raised near midrib, and
diminishing toward margins above; minor veins ob-
scure above, obscurely visible to not visible below.
INFLORESCENCES straight to slightly curved, 3
to 5 per axil, bracteoles 9-20 cm long: peduncle
(2.54—12.5 em long, 6-10 mm diam., sometimes
flattened on one side in cross section, green; spathe
15-17.5(23) em long. medium green outside, slight-
ly paler green inside throughout, except the apical
portion white at anthesis, to 1.7 cm longer than the
spadix. elongating somewhat after closing; spathe
tube less than 2 cm diam. when furled, spathe
blade 2.5-3 cm diam. at anthesis; spadix 10.5-15.8
cm long: free portion 7-13 cm long, 6-8 mm diam.:
pistillate portion 6.5-9.5 cm long, to 1.4 em diam.
throughout; fertile staminate portion 6-7.5 cm long,
9-10 mm diam. throughout; sterile intermediate
segment 2 cm long, with a few staminodia scattered
throughout its length, drying ca. 3 mm wide; pistils

to 51, closely spaced except near apex, ovary
3-3.2 mm diam., medium green to dark yellow;
stigma 2.4-2.7 mm diam.; staminodia white, 2.5-
3.5 mm long, flattened near base, subglobular at
apex; synandria 2.6-3.2 mm diam., drying irregu-

Volume 91, Number 4 Croat
2004 Revision of Dieffenbachia

9 mm

+
g
ve
y
pd
^^
{

1

14 mm 30 mm
E

Figure 14. Dieſſe . 1 (Croat & Zhu 77115). —A. Leaf blade adaxial surface.
T xm inflorescence. —(
one cut off to show the 1

Close- -up of pe stioles
-up of female portion of spadix showing pistils and staminodes. y nfructescences,

Annals of the
Missouri Botanical Garden

larly somewhat rounded, margins often irregularly
turned upward. INFRUCTESCENCE with spathe to
23.5 em long, usually orange; spadix, 9-12 cm
long, ca. З em wide; berries orange to red or orange-
red, drying pale yellow-brown, ellipsoid, 7-8 mm
long. 6 mm diam. (the stigmatic area ca. 2 mm
wide); seeds drying dark brown, 6 mm long. 5 mm
3 mm thick,
outward on funicular side.

diam., to moderately smooth, caved

Distribution and habitat. Dieffenbachia isthmia
ranges from Panama to Colombia (Antioquia and
Chocó). The species is highly variable ecologically,
occurring principally in Tropical moist forest (T-mf)
and drier parts of Premontane wet forest (P-wf) life
zones at 50-800(1000) m elevation, but also in Pre-
montane moist forest (P-mf), Premontane wet forest
(P-wf), and Tropical wet forest
(Holdridge, 1967) in Colombia. In

(T-wf) life zones
Panama, me
species ranges from Veraguas Province to
Azuero Peninsula in the west (200:900 m in саа `r-
rera and Los Santos Provinces).

Phenology. Flowering for D. isthmia occurs in
the early rainy season from May to September (rare-
ly in November), with fruits maturing during the
dry season and early rainy season of the following
year, mostly in April and May, but with many col-
lections made in fruit from August to October.

Discussion. The species is characterized by its
moderately small (usually less than 1 m tall and
with stems usually less less than 2.5 cm diam.)
habit and frequently subcordate blackish-drying
blades which often have a white streak on the distil
half of the flattened (not flat-raised) midrib. In Pan-
ama, it is probably most easily confused with D.
killipii, which differs in having proportionately nar-
rower (typically only to 16 em), usually subcordate

greenish-drying blades with the upper midrib
weakly flat-raised rather than merely flattened
above,

Though its range does not overlap with D. isth-
mia, D. oerstedii may be confused with this species.
'The latter,
differs in having a usually sharply sulcate petiole
and blades that dry
rather than blackened as is usually the

ranging from Mexico to central Panama,

greenish to. vellowish green
case in D.
isthmia.
Etymology.
fers to its dominance

The species epithet “isthmia” re-

Panama.

Кел PANAMA. Canal Area: Barro Colorado
‚ Aviles 24 (МО), oy 397 (MO) Lutz Trail.
ЭТЕП, Croat 10133 (MO),
. Croat 7712 (MO),
Croat 11291 (V, NY, SC Z), Croat 514 83 (MO), Croat 10982
(MO, SCZ), Croat 5709 (MO), Foster 865 (DUKE), Luteyn

in the area of the Isthmus of

x Croat 906 (DUKE), Croat 15173 (MO), Croat 5819
MO). Croat 6308 (MO), Croat 6502 (MO, PMA), Croat
1570 (MO), Killip 39979 (US), Kenoyer 188 (US); 12 mi.
S of Colón on Río Providencia.
(PMA); Frijoles vic., Pittier 3754 (US), В
,atun. Lake, Standley 11107 (US), cdd 40960 (US).
Maxon et a 6812 (US), Maxon et al. 68 0 (US ). Standley
31266 ( TA B above East dis Standley
29807 t Colón: Río Guanche, ca. 5 km upstream
rd. to Portobelo, iid & Trainer 14767 (MO).
: PN Cerro Pirre, vic. Río Perisenico, Croat & Zhu
77115 INB, MO); 112 mi. P of Bayano Dam Bridge. vic.
Canglón, Antonio 4546 (MO, PMA): trail from Cana to
( 170 border along Rio Setgandi. aa et al. 28574
COL, MO); El Real- с Duke 501. 1(МО);:
of B Fe, Tyson et al. 4631 (86 Z),
mi. E of Santa Fe,
rién, between Río Topalisa & Río Pucuro, ca. 17 5o
Pucuro, La Laguna area, Hammel et al. 16262 (C AS, 0 OL
Cana gold mine area, Croat 38010
S of El Real, Alturas de Nique, near
C ana mine, rd. e Boca de Cupe, McPherson 11591 (MO);
ana region, 5 km from Cana trail to Boca de Сире,
McPherson 2s (MO). Herrera: W of Las Minas, near
Chepo, on Montosa de Chepo, McPherson 10958 (МО);
Dist. Las Minas, Chepo, loma El Montuoso, Galdames el
al. 1626 (MO, PMA, US); Las Minas, base of El Higo.
Galdame s et al. 2486 (PMA, US). Los M | oma Prie-
ta, Cerro Grande, Lewis et al. 2195 (COL, DUKE, MO,
UC). тое Distrito С hepo, Puerto C Sie ылай
& De igado 1336 (PMA); San José Island, /. Johnston 1165
. Bayano Lake dam near Canita. Gentry & Tyson
‚ Lewis el
mi. E of Río Ipett, Рие slop 8

—

pm

upstre am 1955 wate tall, near 2 of в 91 Lal Croat
34745 (MO); Is е ти Garibaldi 68 (MO); near Chi-
man, ca. ч mi. up Río La Maestra, Kennedy 1193 (F).

Veraguas: near dicant route of rd. from El Cortezo to
Arenas, Hammel 5378 (MO); Azuero Peninsula, trail be-
tween. Jobero and headwaters of Río Pedregal, Croat
34475 (COL. К, MO, РМА); 18 km W of Las Minas, Cerro
Alto Higo, Hammel 4298 (MO); “Los Girasoles,” Escuela
Agricola Alto a. ca. 5 km NW of Santa Fé, Dressler
47. 16 (DUKE, F. MO, PMA); 18 km W of Las Minas, Cerro
Alto Higo. ra 4298 (MO); Cerro De ae just NW
of Cerro Tuté, S of Santa Fe, s 4043 (DUKE); Dist.
Montijo, dé Coiba, Cerro de La Torre, Galdames et al.
: Isla Coiba, Río Escondido vic.. Galdames et
al. 2252 o. COLOMBIA. Antioquia: Mutat ee
Nuevo Oriente Road, Brand & Ascanio 277 (COL). Cho-
có: Ríosucio, PN Natural Los Catios, Campame а Til-
upo, Forero et al. 1723 (COI 0

15. Dieffenbachia еы Croat, sp. nov. ТҮРЕ:
Coclé: of El Valle de Antón, La
Mesa, forested fat: area near Finca Macarenita,
8?36'N, 80%07'W, 800 m. 6 July 1994
Croat & G. Zhu 76666 Meana à
04612287!; isotypes, AAU!, BI. CAS!
CRI. DUKE!, Fl. GH!, HUA!, INB!, Kl. M!.
MEXU!, NY!, PMA!, SCZ!, US!, VEN!, WU!).
15, 28B

Panama.

Figure

Planta terrestris, 40-100 em.: internodia 1.5-5.5 cm

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

(

70 mm

mm

H

Figure 15. i 7 killipii. 2 Habit showing plant with quilted primary ie veins (Croat Т? —В.
Leaf blade adaxial surface (Croat 78247). C, Close-up of adaxial surface of blade (Croat 74759). . Habit of
ii ring plant (Croat Ў} К, G. (Croat 75154). к Close-up of stems. —F. Habit of Plan ring plant (С) roat 76666).
— Clade: -up of two inflorescences, one at anthesis. —H. Close- -up of pistillate and sterile staminate portions of spadix
7 05 76259).

*

722

Annals of the
Missouri Botanical Garden

longa, (0.8)1.5—3(4) cm diam: petiolus (4)6—20(24.5) cm
longus, vaginatus 2/5 longitudinis vel fere omnino; lamina
oblongo-elliptica vel oblongo-ovato, (13)19-30(33.5) cm
bon (4.5)7-16(21.3) em lata, nervis primariis lateralibus

1-12 utroque; inflorescentia 14 in quoque axilla; pedun-

5 4.5-9 em longus; spatha 12-19 em longa; spadix
12-15 em longus; pistilla 20-37.

Medium-sized herb, 40-100 cm tall, stem creep-
ing over surface of ground at base, then erect; sap
milky, unscented; internodes initially weakly glossy,
often faintly dark green and medium yellowish
green-marbled at lower nodes, becoming glossier in
age, 1.5—5.5 em long, (0.8)1.5-3(4) cm diam., me-
dium to dark green or olive-green or black-green,
drying dark yellow-brown to orange-brown, rarely
dark brown, epidermis sometimes fissured in a
cracked network so as to appear corky in some ar-
eas. LEAVES
apex; petioles (4)6-20(24.5) em long (averaging
12.2 cm long). firm to spongy, slightly paler or dark-

scattered along stem, denser near

r than stem, medium green to dark green, matte
to weakly glossy, faintly striate toward the base,
drying greenish to grayish yellow to brown, sheath-
ing for / to fully throughout (0,4—1 the petiole
length ub averaging 0.69); sheath 3-18 cm long.
(averaging 8 cm), with the sheath margins not dry-
ing markedly different than the remainder of
sheath; sheath apex with the tip free-ending and
inequilaterally acute to emarginate, sometimes dry-
ing acute; unsheathed portion C-shaped and sharp-
ly sulcate to narrowly and sharply sulcate to sub-
terete and weakly sulcate or obtusely and narrowly

sulcate in cross section; blades oblong-elliptic te
oblong-ovate, rarely narrowly ovate, (13)19—
30(33.5) X (4.5)7—16(21.3) cm (averaging 25 X 11
cm), 1.5—4.2 times longer than wide, as long as or
up to 4.8 times longer than petiole (averaging 2.3
times longer than petiole), inequilateral, one side
0.5-1.5 em wider than the other side, sometimes
faleate, subcoriaceous to weakly coriaceous, mod-
erately bicolorous, acuminate to gradually acumi-
nate at apex inequilateral, sometimes inequilater-
ally rounded to subcordate, rarely acute at base:
margins moderately straight on one side, frequently
markedly undulate on other side; upper surface se-
miglossy, dark green, frequently white, pale green
yr yellowish green-spotted or white-streaked, dry-
ing dark brown to olive-brown or gray-green: lower
surface paler, matte to weakly glossy, drying yellow-

~

brown: sinus less than | em deep, rarely to 2.5 em
deep; midrib flat-raised, 3-5 mm wide, sometimes
suleate toward base, usually in moderately deep
valleys, usually concolorous, sometimes paler than
surface above, sometimes weakly 3- to 4-grooved

on upper surface, drying flat-raised to broadly con-

vex, slightly paler to concolorous above, thicker
than broad and narrowly rounded to almost round-
raised, matte, paler than surface to almost conco-
lorous below, drying brown with ridges, darker than
surface below; primary lateral veins 8 to 12 per
side, arising at an acute angle, then spreading at
mostly (40°)45°—70° angle (rarely to 30°, sometimes
to 80° toward base, rarely to 110° at base), fre-
quently forming collective veins that merge with the
margin higher up on the blade, narrowly sunken to
weakly quilted-sunken above, thicker than broad to
convex and weakly pleated-raised, darker than sur-
асе to almost concolorous below, usually drying
darker than
above, obscurely visible and darker than surface to
moderately distinct below. INFLORESCENCES 1
to 4 per axil; bracts 9-20 ст long: peduncle 4.5-9

surface; minor veins few, obscure

em long. 6-7 mm diam., medium green, white at
base; spathe 12-19 cm long at anthesis, 1-2 cm
longer than the spadix, medium green throughout,
sometimes faintly dark green-lineate on faded areas
outside, slightly paler and glossy inside; spathe
tube 2-3 em diam. when closed, 5.5-7.5 cm wide
when flattened, 1.5—2 em diam. at constriction (flat-
tening 3.54 em wide); spathe blade 2.5-3 cm
diam.; spadix bluntly pointed, weakly protruding
forward at anthesis, 12-15 cm long; free portion
5.5-6 cm long (sometimes with a few pistillate flow-
ers in the basal portion); pistillate portion 5-8.5 cm
long, 10 mm diam. throughout; fertile staminate
portion 4.5-6.8 cm long, 7-8 mm diam. midway,
sometimes bluntly pointed (frequently with the
withered portion weakly protruding out of the front
of the spathe after anthesis); sterile intermediate
segment to ca. 5 mm diam., but usually absent with
the pistillate and staminate portions almost contig-
uous; pistils 20 to 37, well-spaced, sometimes ag-
gregated into weak rows, frequently irregularly
gapped, 2 or 3(6) dispersed across spadix width,
widely spaced at base and at apex, pale yellow-
green, 2.4 mm diam., 1.4 mm high; stigma 1.8-2.2
mm diam.; staminodia very thickened and mostly
joined at base, tapered gradually toward apex and
not markedly thickened, sometimes broadened lat-
erally and apparently consisting of a union of 2
staminodia, sometimes with 2 pistils contiguous
and apparently sharing staminodia; synandria 1.2—
1.4 mm diam., ca. 4 per spiral, irregularly rounded
to 4- to 6-sided, drying widely spaced, the margins
of apex markedly turned. upward. INFRUCTES-
CENCE to 23 em long; spathe orange outside; spa-
dix 9-10.5 em long, 2.5 em wide; berries red to
reddish orange or orange-red, drying pale orange-
brown, ellipsoid, 2- to 3-lobed, 7-8 mm long, 6-
10 mm diam.: seeds 1 to 2 per berry, drying dark

Volume 91, Number 4
2004

Croat 723
Revision of Dieffenbachia

brown, flattened on funicular side, to 4.9 mm long,
4.4 mm diam., drying smooth, 3 mm thick.

Distribution and habitat. Dieffenbachia killipii
ranges from southwestern Costa Rica (Puntarenas)
to Panama and the western slopes of the Andes in
Colombia (Antioquia, Chocó, Tolima, and Valle)
and Ecuador (Esmeraldas, Guayas, El Oro, Pichin-
cha. Los Ríos, and Manabf on the Pacific slope and
in Napo on the Atlantic slope) at 0 to 900 m ele-
vation. In Panama it occurs in Tropical wet forest
(Ewf) and Premontane wet forest (P-wf) life zones
(Holdridge, 1967) and ranges from Coclé Province
to Darién Province in the east. In Colombia it is
known from Tropical wet forest (T-wf) and Tropical
rain forest transition to Premontane wet forest (V-rf/
P-wf) life zones.

Phenology. Flowering occurs in D. killipii
throughout the year, with most flowering specimens
having been made in the late rainy season from
September to November. Fruiting collections were
made mostly during the late dry season and early
rainy season of the following year from May to July.
Few fruiting collections were seen between August
and May.

Discussion. The species is characterized by its
medium stature (to 1 m), slender sulcate petioles
with the sheath inequilaterally auriculate at apex
(and usually ending well below the base of the
blade), and especially by the frequently subcordate
blades (which dry yellowish green) with a flat-
raised midrib. Also unusual for the species is the
near absence of a sterile portion between the pis-
tillate and staminate spadices.

Dieffenbachia killipii is similar to D. leopoldii.
which was described from a cultivated plant of un-
known specific origin, believed to have been ob-
tained in Colombia. Engler saw living material of
this species and illustrated it in his 1915 revision.
While it has very similar leaves, D. leopoldii differs
from D. Killipii in having the pistillate and stami-
nate portion of the spadix separated by a sparsely
flowered. almost sterile section. In addition, while
the upper surface of D. killipii is semiglossy. D.
leopoldii is described as having a blade “velvety
green" on the upper surface in the notes of N. E.
Brown (on specimen of Lehmann 1052), at least
suggesting that the upper surface was matte. Fi-
nally, the midrib of D. leopoldii is described as
white, whereas this is not the case with D. killipii.

Collections from the eastern slopes of the Andes
in Napo Province, Ecuador, appear also to be this
species but more studies are needed to confirm this,
as they would be the only collections of D. killipii
in the Amazon basin. The collections include Croat

50480 and Plowman & Davis 4094, both collected
1410 and

1743 m, respectively, and Croat 72573 south of
Coca at 300 m.
by Tan, Halton, and Besse at the Auca Oil Field at

along the Baeza to Tena Road, at
An unvouchered collection made

240 m is also the same species. It has been vouch-
ered from the Marie Selby Botanical Gardens’ liv-
ing collection (SEL 79-0090) by Plowman 14121
and Ingram 1124.

Gentry et al. 65306, from Quindío Department,
Colombia, at 1400 m, may also be this species. but
it is from higher elevation than other Colombian
collections. A collection made in Venezuela at Mai-
quetía at 30 m near the Caribbean (André 4574)
appears to also be D. killipii. However. this may be
questioned because Andre 457 was labeled as hav-
ing been collected in Colombia at Angostura de
Honda (Tolima). Both collections were dated De-
cember 1875

In South America the species may be confused
with D. enderi, described from the valley of the Río
Cauca in Colombia. That species is similar in hav-
ing the petiole sheath auriculate and free-ending at
the apex, and in having the staminate and pistillate
spadices contiguous. It differs in having a thicker
(to 8-9 em diam.
with acute bases and more numerous primary

—
7

stem longer blades (to 50 cm

М

long

aleral veins (ca. 24 per side, spaced 1.5-2 cm
apart). In contrast, D. killipii has blades that are
rounded or subcordate at the base. and fewer than
15 primary lateral veins. It is also similar to D.
daguensis from the valley of the Río Dagua in Valle
Department, which similarly has staminate and pis-
tillate zones contiguous on the spadix. That species
differs in having larger blades (to 40 ст long) with
many close primary lateral veins (up to 25). and a
petiole only 5 em long.

Dieffenbachia killipii is probably most easily
confused in Central America with D. isthmia, which
differs in having stems that dry usually blackened:
somewhat more ovate, blackened blades: and a spa-
dix with a more or less sterile portion between the
staminate and pistillate portions. The species may
also be confused with D. oerstedii from Costa Rica
and western Panama. That species shares leaves of
similar shape and size, but it has blades that are
matte, rather than semiglossy, on the upper surface
and dry greenish or yellowish green. In addition,
D. oerstedii has petioles that are typically more
sharply sulcate than those of D. killipii. The petiole
base is green in D. killipii and whitish in D. oer-
stedii. Furthermore, the spadix has staminate and
pistillate portions nearly contiguous in D. killipii,
but separated by a distinct sterile portion in D. oer-

stedtt.

Annals of the
Missouri Botanical Garden

In Panama the ranges of D. oerstedii and D. kil-
lipii do not actually overlap, but come close in Chi-
All
known collections there occur in the mountains at
900 to 1300 m. Dieffenbachia oerstedii occurs in
Panama in western Chiriquí Province at highland

riquí on the western slopes of the country.

sites and with an outlying population at El Copé in
Coclé Province, while D. killipii ranges in general
no further west than the Azuero Peninsula and Ver-
Panama. There is an unusual
outlying population of D. killipii in the area of the
Osa Peninsula in Costa Rica (Kennedy 1594). A
collection from Cerro Colorado (Croat 48437) in
Chiriquí Province has blades slightly larger than

aguas Province in

most specimens of the species.
74789 from La Mesa in Coclé Province,

is unusual in having a series of rather

Croat
Panama,
prominent collective veins and in having the minor
veins distinct when fresh (typically they are rather
obscure). It was, in fact, so unusual that it was ini-
It is, however,
within the degree of variation for D. killipii.

Kress 77-830 and 77-831 from the vicinity of
Santa Fe
tions in having the staminate and pistillate portions

tially mistaken for a Xanthosoma.

in Veraguas, Panama, are unusual collec-

1
this regard they are similar to D. lutheri, but differ
from that species in lacking the granular puberu-

of the spadix separated by as much as | cm. |

lent major veins on the lower blade surface.

Some collections of the species from Darién
Province, Panama (e.g.. Antonio € Hahn 4405,
Duke 15591, Polanco 1485, and Schmalzel 1212),
are unusual in having petioles more fully sheathed,
sometimes to less than 1 em from the base of the
blade or even with the petiole sheathed throughout.

The Costa Rican population of D. killipii is note-
worthy in that the single collection made there in
the Osa Peninsula is quite disjunct from the nearest
population in Panama, where the species has not
been collected west of Coclé Province. The species
is to be expected at other sites in Veraguas and in
Chiriquí Province, Panama.

Etymology. The species is named in honor of
the late E. P. Killip, botanist at the U.S. National
Herbarium and one of the more prodigious plant
collectors in the Neotropics, who was one of the
earliest collectors of this new species.

Paratypes.

E

COSTA RICA. Puntarenas: Osa Penin-
sula, 2.5 mi. SM

W of Rincón, Kennedy 1594 (MO). PAN-
AM cas del Toro: Cerro de Boc atorito, Peterson &
Annable 6768 (MO). Canal Area: 12 mi. S of Colón, Ty-
son et al. 4486 (SCZ); 12 mi. 5 of C tol6n, near Río Prov-
idencia, Tyson & Blum 3997 (MO, SCZ); Pipeline Rd. 10
mi. from Gamboa gate, Croat 15082 (DUKE. MO): ca. 7—

8 km N of Gamboa, Knapp 2275 (MO); Pipeline Rd. near
1 Clewell & Tyson 3306 (MO, SCZ); Pipeline Rd.

at Rio de Salud, Croat 12353 (MO); Río Pues m Pipe -
line Rd., 1 N of Gamboa, Tyson 1443 (FSU
Frijoles-Monte Lirio, Killip 12154 (US); E E
a el 3 (US): W of the Canal, near * atún, Stan-
К 1 US); rd. S-10 N E E sc ie near junction with
S1. od 12489 (MO); 1.5 mi. N of Escobal, Croat
12191 (MO, SCZ); near Limbo " ‘Club camp, 10 mi. W
of Gamboa on Pipeline Rd., Lazor & Tyson 3492 (FSU);
lake shore along Gatun River perl Pittier 6845 (US):
vie. Gamboa, Pittier 2600 (US); Pipeline Rd. N of Gam-
boa, Kennedy 455 (F). Chiriquí: 8. > km past Gualaca on
rd. to Chiriquí Grande, Hoover 1324 (MO): Gualaca-For-
tuna Dam site, 2.8 mi. beyond b. Planes, Croat 48816
O) Cerro С {айд 15.6 mi. above Río San Felix, Croat

—
=

O). Coelé: El Limón, Me иа 1-10 (РМА),
Mendieta 1-101 (PMA), Mendieta 1-121 (PMA); vic. of El
opé, PN El Copé, 5-6 mi. N of A Copé, below Old

Rive ra saw works area, Croat & Zhu 76746 (CAS, DUKE
МО); 5 hours? duy N from Alto Calvario to 17 Blanco.
Sytsma et al. 1 (MO); La Mesa, above El Valle de
Anton, Croat ye (MO), Croat 14309 (MO); trail beyond
La Mesa towards Los Llanos and the border between Coclé
and Panama Provinces, N of El Valle de
3175 (DUKE), er 37383 (MO);
le, Gentry 7423 ( bh 5 mi.
Luteyn 1203 (DU a а Mesa trail te
coral. NE of Bl Valle de Antón, Luteyn 3180 (DUKE
El Valle, Bartlett & Lasser 16678 (MEXU. МО); Pen "nono-

vide. Croat 67480 (MO, SCZ); г
El Valle, 0.1 km E of Finca E
MO), Croat 74792 (INB, MO, PMA): ca. |
betw. Finca Mandarinas and Finca Furlong, Croat 67197
(MO); area between Cafio Blanco del Norte, Cafio Sucio
and Chorro del Río Tife, Davidse & Hamilton 23599 (MO);
rd. to Coclesito, logg ys e » 12 mi. from Llano 2
Churc hill el al. 4032 (MO), Chure hill et al. 4125 (MO); 7
km N of El Copé, near 1 Sawmill, Folsom & Collins
6436 (MO); La Mesa, above El Valle de Antón, ca. 2 km
W of Cerro Pilón. Croat 37479 (MO, PMA, WU): base of
C erro Pilón red El Valle, Gentry & Daye 364.3 (DUKE,
). Colón: PN Chagres, Sección des rón, Río San
Juan de 5 nf. 1 et al. 361 MA), Espinosa
& Guerra 3762 (PMA), Espinosa et al. 975 (PMA); Dis
Donoso. 5 nto Botija, Polanco et al. 1 905
( o Providencia, 12 mi. S of Colón, Tyson & Blum
3954 (FSU. SCZ); Río ane the, шю sen Puerto Pilón and
е lo, ca. 1.5 mi. S of rd., = X Zhu 76253 (MO,

MA), Croat & Zhu 76259 ino. „ SCZ); lower Río
suanche, Dressler 4688 (PMA); М . ү Guanche, Dav-
idse & D'Arcy 10098 (MO); Río Guanche, 3-5 km above
bridge on Colón-Portobelo Rd., Croat 79329 (MO), Croat

79359 (MO). Sytsma 1658 (MO): near Peluca, km 25.6
from Transisthmian Hwy. on rd. to Nombre de Dios, Ken-
nedy 2661 (MO); ca. 8 km E of dr Thompson 4816
(CM, MO); Portobelo-Nombre de Dios, 1.2 mi. beyond the
jet. of rd. to Isla Grande, Croat 49805 (INB, MO): Nuevo
Tonosi- Río ү 588 lo-Nombre de
MO, ( : Achiote. McPherson 9176 (MO); San-
ta a Rita ridge ae ca. 22 km from transisthmian hwy., Ham-
mel et al. 14472 (MO). Darién: a pio d in

cary) off Río Агей, Duke 13601 (MO); 1-3 N of Pay
Duke & Kirkbride 14019 (MO); de Coc a W hitefoord

E

zi

—.

~

T

Dios, Croat 33551

& Eddy d MEXU. MO): PN Cerro Pirre, vic. head-
quarters on Río Perisenico, Croat & Zhu 77102 (COL.
HUA. INB. L, MO, NY, QCA, SCZ, TEFH, US, VEN):

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

Paya-Pucro, Stern et al. 433 (GH, MO, US); Punta Guay-
abo Grando to Río Jagué. Antonio & е 4405 (MO); :

V Schmalzel 1212 (MO), Schmalzel & m
verson 1199 (MO, PMA): vic. of gold mine at Cana, Croat

IS (HUA, INB. К, MO): S of El Real, headwaters of
E T irre at fork known as Dos n vas, Kennedy & Foster
395 (DUKE): Pinogana-Yaviza, Duke 5169 (MO); 10 mi.
S of El Real on Río Pirre, Duke 5437 (MO); trail from Río
Puero to eee Maskia, Duke n (MO): Río Tucutí
tí, Duke 5260 (MO);
Punta еар Grando-R fo us prse & Hahn 4406
(MO): Cerro Campamento, S of Cerro Рите, Duke 15591
(US): ue ho Frio, halfway up slope of Cerro Pirre from
Piji Vasal, Folsom 6247 (! MO): gold mine at Cana, Sullivan

mi. of Yaviza,

upstream ca. 2 hrs. (piragua) vic.

745 (MO): Bajo Lepe. 7 km al SE of Boca de Cupe, Po-
lanco 146. 3 (PMA) base camp Cerro Pirre МР, Croat
N del Darién.

68961 (C 01. : RENARE
. McDonagh et ral 133 (BM). 439 (BM. bu E st. Biol.
Rancho Frío at N base of Cerro Pirre, ca. 9 km S of El
‚ Quebrada Pe srisenico, de Neve ‘ CAS,

rs et E 0267
na-Coasi trail, R Hartman 12488 (К.
: Río Para, 10 km NE of Jaqué, HA
& биз sma 11198 | MO
Duke 5099 (МО); E Torti, < of Bayano Dam
Bridge, near ‘Torti, Antonio 4638 (MO): Rio Tuque sa, Cle-
zio 221 (MO), 226 (MO); Río pec from Yaviza al junc-
tion with Río Chuc үгүт to y l hr. by — from
jet. Burch et al. 1123 (DAV, NY): 10 km up-
stream from Nazareth, Hahn id y: MO): Ris Jaqué Val-
ley, Knapp & Mallet 3089 (MO); Rio Balsas. Aursar &
Coley 4 (SCZ), 15 (SCZ). Panama: i
near Piria. yr rey (MO):
Saena, 2.5 mi f El Valle de Madroño. 35 mi. y "
turnoff to San е 11.6 mi. N of Las Margaritas, vic.
Chepo, valley of Río Mamoní, Croat bed Zhu 77048 (CAS.
LPB. MEXU, MO, PMA, NY. SEL. S); N of (
Croat 14504 (MO); Cerro Campana, 15 bon SW of Panama
City on Inter-am. Hwy., Mori & Bolten 7698 (MO): ca. 10
km SW of Capira, Mori & Kallunki 3591 (MO), Croat
14706 (MO): above Su Lin Motel, Porter et al. 4282 (MO);
Pan-Am. Hwy.. 3.2 mi. beyond уле еп-
uarda Bosque Station, Croat. 74759 (МЕХ.
MO, PMA, 9 AL). 1 8 Witherspoon 6401 (MO).
Carrasquilla & Rincón 304 (MO), Miller et al. 753 (B.
MO. P MAR PN Campana Buena Vista, Bejuco.
„ E y s et al. . ge along
. Croat 2 (DU KE. МО). dip ec 1593
. Croat 17.
son & Bus 7 (SC WAR
(NY). э
Altos de

—
~
-
8
Iu
У.
a

anita.

0.1 mi. above

Altos de

—

mi. beyond Goofy Lake. d et bel 34(
‚ Sullivan 59 (МО,
3-3.5 mi. NE of Altos de
. y., Croat 68679 (MO): El Llano-Cartí
6.9 km N of Рап- am. Hwy., Folsom 1444 (MO); 4—5
hrs. walk upriver from Torti Arriba, Folsom et al. 6852
(MO). Folsom et al. 60848 ие near Bayano Dam. О Arc)
9420 (MO); Serranía de Majé Trail, Charco Rico-head-
waler of т Río Ipetí Grande. Churchill & de Nevers 4333
ria- -Canasas trail near Piria, Duke 14346 (US):
' Region, vic. Finca Vega, 2.3 mi. Lago
mi. pid old Pa Am. Hwy., Croat 75154
(MO), Croat 11570 (F, SCZ); Río Maje. above first
waterfall, Croat 34442 "n Y^ PMA); Hío Torti, S of Pan-
am. Hwy. near village of Upper Torti, Folsom & Mauseth
7844 (MO). San Blas: SW of Puerto Obaldía. is
16803 (MO): Ailigandí, Hammel & D'Arcy 5018 (MO).
Jones & Tejada 275 (PMA); Kuna Yala Nusigandí FS, Ye

above

-o ~
А,

of El Llano—Cartí Rd., Schatz 1079 (B, K, MO, US). Ver-

aguas: rd. beyond Escuela Agrícola Alto Piedra, NW of
Santa Fé, Pac. slope, 0.6 mi. beyond fork in rd., Croat
19056 (MO): Escuela Agricultura above Santa Fe, Kress

77-830 (DUKE), 77-831 (DUKE). COLOMBIA. Antio-
quia: Rio Anorí valley, Quebrada La Tirana-Providencia,
28 km SW of Zaragoza, Alverson et al. 376 (WIS). Chocó:
Quibdó-Istmina, 6.6 km S of Quibdó, Croat & Cogollo
52174 (COL, a. 10-15 km S of Quibdó. and 8-10
km E, Grayum et al. 7657 (MO); Sautatá, PN de Los Ka-
lios, Por. 10680 (HUA): Río Atrato, Tagachi, Forero
el al. 9007 (COL): Bahía Solano, Corr. El Valle, Quebrada
undo. еа of Río Valle. а et al. ee (MO):
San José del Palmar, Río Torito, Finca “Los Guaduales,”

Forero et al. 6272 (COL), 6489 1255 3 A uds pes vd
de Hondo (Magdalena), Lehmann s.n. (K). Valle: Bajo
Calima E gion. Buenaventura-Málaga, km II.
69543 (СОУС, MO): Pulpapel Headquarters, Bay 27
(MO): 5 pM N of main Cali-Buenaventura Hwy., Croat &
Bay 75707 (MO); Cali, Vereda Pico de Aguila, Gamboa
et al. 71 (MO); Río Dagua, Buenaventura, Lehmann 5311

(К). ECUADOR. Cotopaxi: Guavacan- n-Montene gro, N of
Pucayacu, Croat 73792 (QCNE). rayas: Cordillera

Chongón-Colonche, le, Comm & м
m (GUAY). El Oro: ca. 11 km W of Piñas on rd.
Vrenillas, Thompson 160 (MO); 7.6 9 85 € Tahuin on
rd. to Piedras. Thompson 128 (MO); Machal ja, 25 km
SE of junction in rd. to Piñas, Croat po "ud QCNE).
Esmeraldas: Cerro. Mutiles, Cornejo & Bonifaz 5191
(GUAY); Santo Domingo de los Colorados-Esmeraldas, 90
km NW of Santo Domingo, 8.8 km NW of Quininde, Croat
55549 (MO): 6 km beyond bridge over Río Esmeraldas
(near San Mateo, rd. to oe airport), ca. 6.6 km
beyond Univ. Te ‘hn. Lu
Rio Мише,
San Lorenzo id. Dadi vin et ai 5008 (Е. SE L): Hacienda
ruayas, ca. 20 km S of Esmeraldas, Sparre 15499 (S); Río
Verde, Businga. Juncosa 797 (MO. QCA): Res. Forestal
de Jardin Tropical, Univ. Teenica Luis Vargas Torres, Gen-
try & Lajones 73108 (GUAY, MO): Milan, Quinindé Bilsa
6.1 km W of Sto. Domingo-Esmeralda:
са. 15 km N of Quinindé, Croat et dl.“
MO): Río Lita, Lita, Croat 38947 (F, MO. ; Eloy
Alfaro, Res. Ecol. Cotacachi-C jit i Rio ey Grande,
Y ягу from Centro Chachi de Corriente Grande, varez
P. Herrera 699 (MO, OCNE): He o Vicente, 1 San
Шы. tributary of Río Cayapas, Palacios & Tirado
11327 (MO, ОСМЕ); Esmeraldas-Quininde rd., 40-50 km
SE of Esmeraldas, Harling & Andersson 16727 (GB); Es-
meraldas-Borbón, 2.5 ae W of Borbón. Croat 71119
(QCNE). Guayas: Naranjal-Machala, 13 km S of Naran-
jal, Harling &. Andersson. mer (GB); Canar- Chimborazo.
vic. мар Camp E-3653 (MO, NY, SEL); Cord. Chongón-
117 e Protector Loma Alta, Cornejo & Bonifaz
МО); Loma Alta, Cornejo & Bonifaz 5210
? : Capeira, km 12 Guayaquil to Daule, Dodson
& Dodson He 30 (MO, SEL): = Libertad, Camp E-.
(MO, NY). Los gs El Centinela, Montañas de Па. Pa-
tricia Pilar-24 de 3 et al. 8415
rns Santo e i Esmer aldas hwy.,
. Croat 50684 (MO); Santo Domingo de Los
4 ancho Brahman, ca. 10 km NW of Santo Domingo, Spar-
re 14122 (S); Hacienda Zaracay, Sparre 15182 (S), Acosta
Solís 10896 (F, S); Tsachila Chiguilpe, Cerón et al. 29159
AP): Santo Domingo-Quevedo, km 11.5, Est. Gustavo
Orcés, Quishpe & Dávila 82 (QAP, ОСМЕ): km 41, Zak
et al. 5726 (QC A); vic. of Montalvo, 40 km E of Babahoyo,

oe

Y
©

—

726

Annals of the
Missouri Botanical Garden

Holm-Nielsen et al. 2769 (AAU, NY, QCNE, 5); Hacienda
Monica, 12 km E of San Carlos, Sparre 19397 (S); Haci-
enda PEE. Harling 313 (8); Babahoyo- e
S). Cornejo & Bonifaz 4828 (G ‚ МО);
alenque, Croat 38669 (MO,
SEL), Croat Qoo (MO,
Р 5 (МО), Fallen & Ray 860 (SEL);
Quevedo; Asplund 15574 (S), Dodson 6188 (RPSC, SEL);
inces, Mocachi-Palenque, Jauneche forest, km 70 Quev-
-Palenque, via Mocachi, Dodson et al. 10594 (GUAY,
SEL). Manabi: Portoviejo— Pichincha rd., ca. 20 km

E a San Plác ida. iab. Aas & Andersson 24778 (С В, МО);
Cerro Montecristo, anta, Sparre 19488 (S); Mach-
alilla NP, zona de S Se sbi data Gentry et al. 72496 (MO,
QCNE); Chone- Santo Domingo Rd., ca. 20 km NNE of
Flavio Alfaro, Montañas de Convento, Harling & Anders-
son 18898 (GB); Hacienda Don Juan, 10 km NE
N of Rfo Don Juan, Neill et al. 11683 (QCNE);
of Pedernales, 3.5 km SW of Camarones, Pide 452
U, NY, MO). Napo: Auca, d 14121 (F). Pas-
taza: Coca-Río Tiguino, 85.8 km S of Coca, Croat 72573
(MO). Pichincha: vic. Hotel Tinalandia, 9.6 km E of San-

"d

"rA

eis d a 755 75 1104 (MO); Centinela, Mon-
e Па, 1 E of Patricia Pilar, Lojtnant & Molau
(AAU); Saal 10 7 d do, Patricia Pilar.
i. al, 14638 NE), Gentry et al. 26709

О); vic. of Santo E р Los Colorados, ee
SW of Santo Domingo, Croat & Nuñez 82064 Se
QCNE); Nanegalito-Pto. Quito Rd. km 113, ENDESA, :
km W of San Vincente Andoas, Croat 82829 (MO), ы
et al. 83795 (МО); Rio 510700 she, Quito-Pto. Quito, km
113, i da 262 ( QCA); Santo Domingo—Quininde
rd., km 41, Zak et al. 5414 (QCA); vic. pes lar tg
Res., rd. » Maquipue una Lodge, Leimbeck R. 306 (AAU).
Sucumbios: Lago Agrio-Baeza, ca. km i Dd 50480
(MO). VENEZUEL = Maiquetia, Andre 457 (К).

Cultivated specimens. Ecuador. Napor a а Oil Field,
23 Sep. 1991, pupila 1124 (MO).

Z
<

16. Dieffenbachia longispatha Engl. & K.
Krause, Pflanzenr. IV, 23 Dc(Heft 64): 44.
1915. TYPE: Panama. Colón: Fato (Nombre de
Dios), July 1911, H. F Pittier 3838 pape
US!; isotypes, B!, F!, MO!). Figures 16, 29

Terrestrial, (1)1.5—3.5 m tall; sap very foul and
pungent; stem prostrate at base, then erect; inter-
nodes 4—12 cm diam., with leaf scars prominent,
dark green, semiglossy, drying dark brown to or-
ange-brown; petioles thick and succulent, semiglos-
sy, usually solid dark green, rarely streaked with
pale green, 23-55 cm long (averaging 36 cm long),
sheathed to about middle (0.58—0.85 their length,
averaging 0.72); sheath 25—41 cm long (averaging
25 cm long), inequilaterally rounded at apex, some-
times weakly free-ending; unsheathed portion 4.0—
30.5 cm long (averaging about 11 em), C-shaped
and obtusely sulcate or + terete with a faint flat
rib adaxially; blades 1 8 75 -е 1 8 41-72 х 17-

em (averaging 53 X 2 , 1.7-2.9 times lon-
ger than wide (averaging 23 times longer than

wide), 1-2 times longer than petioles, coriaceous to
subcoriaceous, semiglossy, bicolorous, weakly in-
equilateral, one side 0.6-3.5 cm wider than the oth-
er, usually short-acuminate at apex, sometimes
acule to rounded with a short acumen, acute to
rounded at base, with the edges turned up near the
base; upper surface dark green, drying gray-green
to dark olive-green, rarely yellowish brown; lower
surface slightly paler, drying yellowish green, rarely
yellowish brown; midrib flat, 1-2 cm wide at base,
concolorous or slightly paler than surface above,
drying slightly paler than surface and weakly raised
above, concave to prominently raised on lower sur-
face, drying brownish; primary lateral veins 15 to
26 pairs, sunken above, convex below, arising at an
acute angle to the midrib then spreading at an an-
gle of 45°-60°(70°), sometimes to 90° near the base
of the blade, sometimes drying moderately wrin-
kled; interprimary veins lacking or 1 between each
pair of primary lateral veins, sometimes almost as
prominent as the primary lateral veins; minor veins
indistinct. Juvenile blades with acute base and sol-
id green midrib. INFLORESCENCES 1 to 3 per
axil; peduncles (5.5)7-25 X 1.5-2 cm; spathe
medium to dark green, broadly curved, long-acu-
minate, 27—48 cm long, 2.5-8.2 times longer than
peduncle, to 4 em wide at anthesis, tube flattening
5-12.5 em wide, constricted area 2.5—3 cm diam.,
flattening 3.2-5 cm wide, spathe blade 3-6 cm
wide at anthesis, flattening to 6-12 cm wide mid-
way, the distal inner surface sometimes white when
open; spadix (21)35—38 cm long; free portion 12—
19 cm long; pistillate portion of spadix (except
sometimes the uppermost part) fused to spathe, 13—
15 cm long; fertile staminate portion (8)1 1-14 ст
X (9)12-14 mm (drying 6-9 mm diam.); mostly
sterile intermediate portion (2)3—4.3 cm long with
a few scattered staminodia in the upper half (some-
times to throughout its length); pistillate flowers 10
to 26, round or barely bilobed, widely spaced, 5-
10(20) mm apart, forming in a single irregular row
or scattered but usually no more than 2 flowers
across the width of the spadix (rarely 3); ovaries
pale green, 4—7 mm diam.; stigmas 4—6 mm diam.,
yellow to orange, somewhat broadly bowl-shaped,
5-7 mm thick on the edge, medially with 1 to 2
somewhat elongate lobes, 1-1.5 mm
somewhat longer than broad; staminodia 5
2-3 mm,

the lobes
diam.,

to 6 per pistil, white, irregular, 2-6 X
much flattened at base, less so toward the apex,
often somewhat puckered at the apex; synandria in
spirals of 4 to 7 each, 3—4 mm wide, subrounded,
drying light yellow-brown and concave at apex. IN-
FRUCTESCENCES 17-24 cm long; berries 1.5-2
em diam., often deeply emarginate at both ends ш

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

Figure 16. d ا‎ —A. Habit with open inflorescence. —B. Plant habit with cluster of inflo-
rescences. —C. Crown of plant with close-up of leaf base with open inflorescence. —D. Inflorescence at anthesis with
staminate spadix exposed. 45 C. ye & Zhu 76257); B, D. (Croat & Zhu 76203).

728

Annals of the
Missouri Botanical Garden

appearing to be a double fruit, bright yellow to or-

ange; mesocarp ca. 2 mm thick,
tasty at maturity; seeds oblong,
brown to black, smooth.

soft,

Distribution and habitat. Dieffenbachia longis-
patha ranges from central Panama to northern Co-
lombia, mostly from sea level to 180 m, but perhaps
to 250 m (owing to a collection at Río Tuquesa with
no elevation reported), occurring in Tropical moist
(T-mf), Premontane wet (P-wf), and Tropical wet for-
est (T-wf) life zones (Holdridge, 1967). In Panama

it occurs on both coasts, but it is relatively rare on

While collections of D. longispatha
have been made in both flower and fruit vear-round,
flowering occurs principally during the first half of
the rainy season between June and August, while
fruits mature throughout much of the dry season
and the first half of the rainy season, especially
from February to September.

Discussion. Dieffenbachia longispatha grows
most frequently along streams, in deposits of sedi-
ment along lakes, in standing water, but also in

deep soil in the forest understory. Frequently it is
found solitary or in small clusters. While the spe-
cies may colonize, it is typically much less colonial
than other species in Panama and Colombia, such
as D. isthmia, D. oerstedii, or D. killipii.

The species is characterized by its usually tall
((1)1.5—3.5 m high) and robust stem (usually 6-12
em diam.), and by the petiole being
ously sheathed and decurrent at the apex with a
long subterete free portion beneath the blade, this
drying characteristically olive-green or dark brown,
Perhaps most characteristic of D. longispatha are
the widely scattered, moderately sparse and very
large pistils and the usually long spathe. Dieffen-
bachia longispatha is typically one of the tallest
species (to 3.5 m) with the thickest stems (to 12
cm diam.) in Central America. Only some plants of
D. panamensis and D. aurantiaca often develop
plants of comparable stature, but one collection of
D. standleyi (Madison 705), with stems to 2.2 m
tall and 9-11 em diam., is reported.

The species has long been confused with D. ni-
tidipetiolata, which ranges from Nicaragua to Ec-
uador.

INCONSPICU-

—

That species differs in having a typically
somewhat smaller stature (usually 1—1.5 m tall).
petioles that are in general very glossy, and pistils
that are moderately small (to 3 mm) and closely
aggregated. Dieffenbachia nitidipetiolata also has a
different beetle pollinator scent at time of flowering
according to observations made at La Selva in He-
redia Province, Costa Rica, D.

by Beath (pers.

sweel and
7-8 mm diam.,

comm.). Dieffenbachia longispatha and D. nitidi-
petiolata do not occur together in Costa Rica since
D. longispatha barely crosses west of the Panama
Canal. In eastern Panama D. longispatha is found
principally in areas of Tropical moist forest (T-mf)
near El Real.

Smaller plants of D. longispatha may also be
confused with D. crebripistillata. In addition to be-
ing a plant of smaller stature (rarely to 1.3 m tall),
it has more fully sheathed petioles (often to the
base of the blade and sometimes overlapping the
blade) that usually have a whitish band abaxially
and dry conspicuously yellow or orange-brown (vs.
green for D. longispatha). In addition, D. crebripis-
tillata differs in having smaller spathes (to 28 ст)
with the pistils closely aggregated on the spadix,
with (57)80 to LOO pistils versus 10 to 26 for D.
longispatha. Finally, though there may be a certain
overlap in their ranges in areas along the Atlantic
coast in Colón Province, D. crebripistillata generally
occurs at higher elevations, mostly 250 to 975 m.

5

о examined. PANAMA. Boeas

del Tor cm N of La Gruta, Peterson 6405 (US).
Canal ae Baro а Island, кез Trail 2000,
; Barbour Trail 225, Croat 6471

Croat 11321
(

МО); Barbour Dm A Croat 7136 (M

5 Trail.

near end. Croat 5767 (MO); Drayton Trail 1610. Croat
5761 (MO); Lake Trail, Croat 6276 (MO, SCZ): Oppen-
co 67-1-3-1244 (MO); Miller Trail 300, Croat 4095
(MO); Miller trail 1400, Croat 17394A (MO): Miller Trail
1: a Croat 7455 (MO); Pearson Trail 400, Croat 4134
(MO); Snyder-Molino Trail. Croat 6192 (MO): Van Tyne
Trail, Stimson n (DUKE, STRD; Wheeler Trail 300,

J

Zetek Trail 500, Fuertes Cove,
19 5 0.6 mi. N of Gamboa near
. Curundu Housing area

of Albroo 5 Ше Metropolitano, Croat
& Zhu 76203 (AAU, CR, MO, US): Gatun Locks-Fort
Sherman, 1 mi. E of Fort Sherman, Croat & Zhu 76266
(MO, US): Río Grande-Pedro Vidal, rd. to Arraijan, Pittier
2715 (US) near Fort Randolph, Standley 28732 (US);
Madden Forest ca 3 mi. from Mac n Wye, Croat 33018
эч, Р, РМА); . Croat 12319 (MO,

Rio Casaya adi ‚ 6 km
Do (F, MO). Colón: Río Gane the, Puerto Pilón-Porto-
belo, 6 km S of و‎ lo, ca. 1.5 mi. f rd., Croat &
Zhu 76256 (COL, ), PMA, RSA), 1 (COL, HUA
MO, PMA); Rfo 1 A upstream, Croat 75195
(MO), Croat 11411 (MO). Darién: PN Cerro Pirre, vic. of
0 along Rio Perisenico, Croat & Zhu 77101 (CM,

STRI, US); tributary of Río Tuira, upstream from El Real,
MeDade s.n. (MO); PN Darién, y rro Pirre base camp, Río
Parac Pe be те (MO); 3 mi. E of Santa Tyson
et al. < ; Río 19 headwaters, ca. em air
Rn 'e der С E Divide, Kittridge gold Pid camp.

; of Gamboa, Nee
5

Croat 27196 (MO); Upper Río Tuquesa, LeClezio 135a
(MO). Panamá: 5 mi. above Interam. Hwy., rd. to Cerro
Azul, Croat 11. (MO, SCZ); EI Valle de Madrofio-La
Saena, 2.5 mi. N of El Valle de Madrofio, Croat & Zhu
77042 Т ; 5 mi. № of Chepo, Tyson 6700

(MO): Río Majo- (ерга Brava, Croat 34654 (МО); El

Volume 91, Number 4
2004

Croat 729
Revision of Dieffenbachia

Llano-Cartí. Rd., near is
Croat. 673994 (MO); Río Tapia, Standley 26156 (US
Standley 28238 (US). San Blas: E of Puerto Obaldia.
Croat 16923 (MO). COLOMBIA. VES ee
Guillermo & yat L. 863 (HUA, JAUM). Choco:
Acandí, Río Cuti, Corr. Unguia, Romero-Castaneda 6436
(COL); Nuquí. p Arusí. vic. Arusí, Río Arusí. Croat &
M. Mora 83777 (= Mora 394) (MO). Meta: PN Natural
Tinigua, Serranía Chamusa, Centro de
matológica
(COL).

with San Blas Province,

Investigaciones Pri-
s La Macarena, Camp Colombia, Stevenson 379

17. Dieffenbachia lutheri Croat, sp. nov. TYPE:
Panama. Chiriquí: along border of Bocas del
Toro Province, Cerro Colorado, above mine.

1600 m, originally collected by Luther et al.,

cultivated at Marie Selby apad Gardens

(acc. 486-0873). 4 Oct. 1991. . Ingram
1146 (holotype, MO-42243501: prd, B!,
COL! Kl. MEXU!, PMA!, SEL-065912!, US!).

Figures 17, 27B.
Planta

diam.;

0.6-1.5 m alta;
petiolus 23 em longus, pd tus 0.7 longitudinis:
lamina anguste ovata, (2: AT lem longa, 14—15 em lata,
nervis primariis late ralibus i E utroque; inflorescentia

per axillam: pedunculus 4-6 em longus. | em diam.:
Spatha pallide viridis, 16.5-20.5 ст longa.

мей енын brevia, 2.0-2.4 en

Herb. 0.6-1.5 m tall; sap not smelling of oxalic
acid; internodes short, 2.0-2.4 cm
diam., dark green and semiglossy, drying matte and
blackened; petioles ca. 23 cm long, dark green and
weakly glossy, smooth or with fine, obscure lines on
fresh material,

to 2 em long.

sheathed 0.7 their length. drving
dark olive-gray toward base, somewhat. vellowish
brown toward apex; sheath acute on one side at
apex, the other side narrowly rounded at apex. with
both sides confluent, the sheath margins drying
thin, pale brown, the inner surface of the sheath
pale yellow-green and very glossy, drying light vel-
low-brown, much paler than the outer surface: free
portion of the petiole oval to sharply C-shaped in
cross section, 7 cm long, sharply sulcate to flat-
tened with sharply ridged margins; blades narrowly
ovate, (24)27-34 X 14-15 1.9—2.2(2.7) times
longer than wide, slightly inequilateral, one side
0.9-1.7 em wider than the other, weakly to narrow-

ly acuminate to acute and apiculate at apex. round-

cm,

ed and usually inequilateral, sometimes acute and
decurrent on the petiole at base, moderately un-
dulate along the margins, moderately coriaceous to
subcoriaceous, very dark green and semiglossy to
weakly glossy above, sometimes mottled in a band
along the midrib (especially heavy on one side be-
low the middle) with yellow-green to cream above.
drying dark gray-brown to dark brown and matte to
weakly glossy above, slightly to moderately paler
and weakly glossy to matte below. drying yellow-

San Luis.

green, weakly glossy; midrib slightly flat-raised,
concolorous and 4—5 mm wide, weakly ribbed and
medially sulcate above, narrowly rounded and
slightly paler below, drying flat-raised and slightly
darker yellow-brown above: primary lateral veins 14
to 16 per side, arising at an acute angle, then
spreading at 25°-70° angle (25°-45° angle toward
the apex, 65707 toward the base), weakly quilted-
sunken to narrowly sunken and concolorous, some-
times in weak valleys above, darker and convex to
round-raised, minutely granular-puberulent to sca-
bridulous below, narrowly

raised, concolorous above, irregularly angular and

drying weakly and
yellow-brown below; minor veins on upper surface
in part weakly etched, concolorous, those on the
lower surface moderately obscure to easily visible,
darker than surface: lower surface densely pale-
spotted, the spots regularly rounded and evenly
spaced. INFLORESCENCE 1 per axil; peduncle 4—
6 cm long. drying dark yellow-brown,
3.5-8 mm wide; spathe pale green on both surfaces,
white near tip, acuminate at apex, 16.5-20.5 cm
long. flattened to 3.5 em wide on tube, drying vel-
lowish brown: spadix 14-20 cm long (including 1—
1.5 em long stipe); pistillate portion of spadix 7.0—
1.9 em X 8-9 mm, completely contiguous with sta-
minate portion or nearly so; staminate portion of
spadix 5.3-8 cm X 5-9 mm on drying, with the

] em diam.,

remnants of thickened thecae visible along upper
margins: pistils 55 to 66, 2 to 4 of them in a spiral
across the width of the spadix. sometimes moder-
ately sparsely spaced, drying sometimes promi-
nently convex and the pistils thus visible from both
top and side views: pistils 1.4-2.3 mm wide: stig-
mas pale yellow, 1.3-1.7 mm diam., drying with
short, mostly acute, mostly erect strigose trichomes:
staminodia 2-3 mm long, 1.0-1.6 mm wide. mark-
edly thickened at the apex, sometimes broader than
long. white, drying yellow-brown; synandria creamy
white, 0.5—

3.0 mm wide, yellow-brown, the apex sunken on

drying irregularly rounded to angular,

drying. medium yellow-brown with pale. rounded.
cellular inclusions. Berries not seen.

Distribution and habitat. Dieffenbachia lutheri
is apparently endemic to the region of Cerro Col-
orado in Chiriquí and Bocas del Toro Provinces at
1390 to 1600 m in the Lower montane rain forest
(LM-rf) life zone (Holdridge. 1967

Phenology. & flowering 1 was made in
Panama, and the species has flowered in cultivation
in October at the Marie Selby Botanical Gardens.

Discussion. The species is most similar to D.
longispatha in having a considerable portion of the
petiole unsheathed and obtusely sulcate: the sheath

Annals of the
Missouri Botanical Garden

ES

—

Figure 17. Dieffenbachia lutheri. — &. Habit of P plant. —B. Plant abi with inflorescence. —C. Close-up
of stem showing petiole sheath and sulcate petioles. Close-up of inflorescence

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

acute at the apex; and a blade of generally similar
shape and dried color. It differs from D. longispatha
in occurring at a much higher elevation (1390—
1600 m vs. 180 m), in having the staminate and
pistillate portions of the spadix contiguous (sepa-
rated by a conspicuous, mostly sterile portion in D.
longispatha), and in having a spathe that is much
shorter (to 20.5 ст vs. 27-48 cm).

Dieffenbachia lutheri is also similar to D. killipii
and even shares with that species the contiguous
pistillate and staminate portions of the spadix. It
differs from D. killipii, however, in having the major
veins on the lower surface granular-puberulent
rather than glabrous.

Dieffenbachia lutheri might be confused with an-
other high-elevation species, D. crebripistillata, but
that species occurs only up to 950 m,
D. lutheri, and differs in having a fully sheathed
petiole that dries yellow-brown. Dieffenbachia luth-
eri has a petiole that dries dark gray and is un-
sheathed for more than 5 cm at apex.

The species is named in honor of

lower than

Etymology.
botanist Harry Luther from the Marie Selby Botan-
ical Gardens, Sarasota, Florida, who collected liv-
ing material of the type species.

PANAMA. Bocas del Toro: Cerro Colo-
rado, 9 W of Chamé, Croat 69070 (MO). Chiriquí:
To d о, 18.6 mi. N of Río San Felix, 6.6 mi. be

ond Chame, Croat 75007 MO); 34.1 km of Río San Fe dix,
Croat 37268 (MO).

Parat y m s.

18. Dieffenbachia nitidipetiolata Croat & Gra-
yum, sp. nov. "E: Panama. Bocas del Toro:
Valle del Silencio, along Río Changuinola, ca.
Teribe
Indian population, disturbed forest among co-
coa plantations, 9?21'40"N, 82%31'40"W, 100
m, 25 June 1994, T. B. Croat & G. Zhu 76449
(holotype, M0-04614032—33!; isotypes, AAU!,
B!, CAS!, COL!, CR!, F!, GH!, INB!, K
MEXU!, NY!, PMA!, US!). Figures 18, 30A.

1 km above mouth of Río Teribe, vic.

pe 50—75(120) em alta; "eor 0.7-1.5 em lon-

‚ 1.5-2.5(4.0) em diam.; petiolus 13—44 ст longus, va-
podran 0.30.76 О vagina 14-34. cm longa,
acuta ad apicem; pars libera 5-22 cm longa; lamina a
longo-elliptica vel oblongo- 5 vel ovato-elliptica,
19-59 cm longa, 7-27.5 ст lata, nervis primariis jet
alibus (10)12-20(22) mir xo inflorescentia 1—5 in
quoque axilla; pedunculus 11-18(24) em longus; spatha

—36 cm longa; spadix 13-29 cm dedi pistilla 48—
60(79).

Herb, 50-75(120) cm tall; sap moderately foul-
smelling; stems erect or partially reclining; inter-
nodes 0.7—1.5 cm long, 1.5-2.5(4.0) ст diam.,
glossy to semiglossy, dark green to medium green,
smooth, drying dark brown to light yellow-brown,

matte, moderately smooth; petiole scars 4—5 mm
thick. LEAVES
of stem; petioles 13-44. cm long (averaging 28.4 cm
long), 1-1.5 em diam. midway, sheathed 0.3—0.76
their length (averaging 0.48), very glossy as if var-

erect-spreading, clustered at apex

nished, rarely only semiglossy, dark green, drying
orange-brown to blackened; sheath 14—34 cm long
(averaging 14.3 cm long), erect to involute, acute
and decurrent (but sometimes weakly elevated) at
apex; the unsheathed portion 5—22 cm long (aver-
aging 13.4 cm long), usually terete to C-shaped,
sometimes obtusely and narrowly to broadly sulcate
or V-sulcate, rarely D-shaped; blades oblong-ellip-
tic to oblong-lanceolate, or ovate-elliptic, gradually
acuminate to acute, equilateral to inequilateral at
apex, usually only weakly inequilateral with one
side 0.3-1.5 em wider (but can be up to 3.5 cm
wider) than the other, acute to obtuse or rounded
at base, usually equilateral, sometimes inequilater-
al with one side acute and the other rounded, 19—
59 X 7-27.5 cm (averaging 38 X 12.6 ст), 2.1—
4.8 times longer than wide, broadest usually at
middle, 0.7-2.4 times longer than petiole (averag-
ing 1.38 times longer than petiole), subcoriaceous
to thinly coriaceous, moderately to weakly bicolo-
rous; margin sometimes weakly undulate; upper
surface dark green and glossy to semiglossy, plain
green or rarely weakly variegated with pale green
in some areas or throughout much of the blade,
sometimes plain green with just the midrib whit-
ened, drying gray-green; lower surface moderately
paler, matte to weakly glossy, drying yellow-green;
midrib + flattened (slightly sunken toward base).
concolorous or slightly paler, sometimes white
above, convex or bluntly acute below, drying pale
yellow-brown often with a medial ridge on drying:
primary lateral veins (10)12 to 20(22) per side, de-
parting midrib at 207—40*(55?) angle on narrower
leaves (especially in Panama), often to 70-85” an-
gle on broader blades (mostly in Costa Rica), weak-
ly arcuate-ascending, weakly sunken above, weakly
convex and slightly paler below; minor veins visi-
INFLORESCENCES

ble, not prominent below
mostly 1 to 5 per axil; bracts 2-ribbed throughout;
peduncles 11-18(24) ст long, 0.9-1.3 em diam.,
somewhat flattened, green, semiglossy:
spathe 15-36 cm long, 1.3-2 times longer than pe-
duncle, uniformly pale green to greenish white or
greenish cream, becoming pale yellow post-anthe-
sis, semiglossy to matte outside, slightly paler and
glossy within, spathe tube 2-2.9 ст diam., flatten-
9 cm wide, weakly constricted above the
the constricted area to 5 cm

medium

ing to
tube to 1.7 ст diam.,
wide when flattened, narrowly acuminate at apex;
spathe blade 2.5—3.5 cm wide at anthesis, flatten-

732 Annals of the
Missouri Botanical Garden

Figure 18. Dieffenbachia иеа —A. Habit. —B. Close-up of leaves, adaxial surface. —C. Close-up «
crown - PY showing ne m ened leaf and inflorescence. —D. Opened inflorescence exposing spadix. A, B. (Grayum
218 ү . D. (C roal 70942

Volume 91, Number 4
4

Croat 733
Revision of Dieffenbachia

ing to (3.7)4.5—5.7 em wide midway: spadix 13-29
em long. ca. 1—9 em shorter than the spathe: the
free portion 11-16 cm long; fertile staminate por-
tion 5.7-10.5 em X 6-11 mm, slightly broader at
middle. gradually tapering toward both ends. blunt-
ly rounded at apex; male flowers 4 to 6 per spiral.
subrounded to hexagonal. sometimes depressed
medially, the margins irregularly and smoothly in-
dented; pistillate portion 5.5-14 cm long. 11-15
mm diam., extending down to the very base of the
spathe; pistils 48 to 60(79) globose, green. to 2.5—
3 mm diam., moderately closely spaced except
sometimes in uppermost | em (the distance be-
tween them generally equaling or up to twice their
width), usually to 3 per spiral or 4 to O in an arch
across the width of the spadix: stigma vellow. de-
pressed-globose, simple: staminodia 3 to 5 per flow-
er, clavate, white, 2-6 mm long, up to 2 times lon-

ger than pistil, somewhat flattened and mostly

contiguous at base (sometimes united in pairs).
sometimes slightly thickened and somewhat puck-
ered at apex, drying orange: staminate portion in-
terrupted from eni portion by a + naked por-
2.5-4.5 em X 5
staminate flowers scattered at both ends or sparsely
half. INFRUCTESCENCES
spathe orange, to 23 cm long; berries globose. bright

4—6 mm diam.

tion, 5-9 mm with a few sterile

in the lower with

red,

Distribution and habitat. Dieffenbachia nitidi-
petiolata ranges from Nicaragua to Costa Rica (He-
redia, Limón) to Panama (Bocas del Toro. Colón.
San Blas), Colombia (Antioquia. Chocó). and Ec-
uador (Esmeraldas and Morona-Santiago). from
near sea level to 1200 m in wetter parts of Tropical
(P-wf).
Tropical wet forest (T-wf), and Premontane rain for-
est (P-rf) life zones (Holdridge, 1967

Phenology.

moist forest (V-mf), Premontane wet forest

©
ex
—

Dieffenbachia nitidipetiolata flow-
ers principally at the beginning of the rainy season
(June-September), but also as early as March and
as late as October, with the heaviest flowering ap-
parently in August. Fruiting collections have been
made from May through January.

Discussion. The species is characterized by its
long. glossy petioles with the unsheathed portion
being moderately elongate, 0.7—0.24 cm of their
length, and which dry glossy as though varnished,
and by the moderately closely spaced pistils. It is
most easily confused with D. longispatha, differing
from that species in having the pistils much smaller
and aggregated and from D. crebripistillata in hav-
ing the petiole almost unsheathed (vs. sheathed
mostly to the apex in D. crebripistillata). The spe-
cies may be confused with D. hammelii. That spe-

cies differs in having a minutely granular upper
surface, a matte-drying lower midrib with promi-
nent raphide cells (vs. drying glossy without raph-

—

ide cells), and matte-drying petioles (vs. drying
glossy)

In the Río Guanche area of Colón Province, Pan-
ama, the species may be hybridizing with D. cre-
bripistillata since both species occur along the Río
Guanche and in the Santa Rita area further inland
and at higher elevations. Some plants have the free
portion of the petiole over half its length on aver-
age, which is characte ‘teristic of D. nitidipetiolata
(but not of D. stillata).
is not notably ы as is usually the case for D.

yet the free portion

nitidipetiolata. Examples of these collections are
McPherson & Merello 8235 from Santa Rita Ridge
and Thompson 4874 from Río Guanche. The Me-
Pherson and. Merello collection also describes the
pe tiole as having a white streak on the abaxial sur-

ace, a feature otherwise known only in D. crebri-
pistillata.

Paratypes. COSTA RICA.

San к beyond ien Ange ч:

Alajuela: 34 km be yond
Luteyn 3.

3.5 km W of Fortuna, 2.5 km N X of New Volcán Are ек
Taylor bh Taylor "oon ood Naranjo-Aguas Zarcas.
along Hwy. 15, m NE of Quesada. Croat 46947
(MEXU, MO); N э of Volcán Arenal, Lent et al. 3374

(F): Cordillera de Tilaran, San Ramón-Bajo Rodríguez.
30-37 km NW of San Ramón, Croat 68195 (CM, К, MO):
15 km WNW of саа by air 2 km W of Jabillos, Lies-
ner et al. 15144 (B. ( ^

Lorenzo-Los Angeles

11198 (E, MO); Rio Pus 8 |, ›
> J^ 5024 (F, US). Ca ee аат Limon, Hwy.
32. ca. 9 mi. NE и Turrialba, Croat 43368 (MO); Gua-

с а s Rd.. Barringer 2416 (F). Heredia: La Sel-
va at Sarapiquí, Jimenez 103 (MO): La Zona uror
Rio Guacimo, Grayum & Schatz 3218 (DUKE): La Selva,
OTS Field Station on the Río Puerto Viejo. E of it
with T “у Sarapiquí. Croat 14254 (MO), Hammel ¢ 8i 23
(DUK . MO). Burger & Stolze 5753 (F, GH). Folsom
m r KE). price 10082 (DUKE). Beach 1436
JUKE). Beach 1439 (DUKE. MO). MacDougal 1027
nu KE), dies 103 Ah Río Sarapiquí. 2 km 5 of San
Miguel, Lent 37 (F); Sarapiquí. Croat 44307 (MO), Gra-
yum 2225 (D m МО); San José and Pto. Viejo. vic. of
Chilamante. 11.6 mi. N of Cariblanco. Croat 15 (MO).
Limón: Hitoy Cerere. reserve, SW of Valle
along Río Cerere to

La Estrella,
= m th from Quebrada
Barrera, Grayum & Hammel 5 5785 (MO); Res. Biol. Hitoy
Cerere, Valle de la Estrella. trail to e ro Bobóca "d. G.
Herrera 4116 (CR, MO); N of Quebrada El Mc lon Río
Chirripó-Río Corinto, Grayum & Jacobs 3524 (MO): Ref.
Nac. Barra del Colorado. Río Chirripócito-Río Sardina.
и 9844 (CR, МО); Río Catarata. Burger et al. 103
SEL); BriBri-Río Sixaola. Río Catarata, Burger y
nes 10905 (F. MO, PMA): BriBri-Caribbean coast,
Croat 43217 (MO). Puntarenas: E of Monteverde on the
Pacific watershed, Burger et e: 10699 (MO); Palmar Nor-
te-Panamerican border, 3 N of turn-off to Rincón.

Croat & D. Hannon 79199. (INB. MO. US). San José:

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Vazquez de Coronado, Braulio Carrillo NP, along Hwy. Sar
José to Siquirres, trail to Río Sucio, site of the Old Carillo
Station, Croat 78788 (IBE, INB, uen WU). NICARA-
GUA. Zelaya: Caño Montecristo, E o 5 Ger-
mán Pomares, P. Moreno & J. ا‎ 15160 (M 0): Rfo
Punta Gorda, Atlanta, “La Richard,” 200 m SE, Moreno
& Sandino 12976 (MO). PANAMA. Bocas del Toro: Río
San Pedro, Gordon 55C (MO); Santa Catalina, x Ds.
1967, Blackwell et al. 2704 (COL, MO, UC); Chiriquí La-
goon area, Cocoa Cay, von ibid 2892 (COL, F, MO, UC);
а КК stop at Milla 7.5, Croat & Porter 16303 (MO),
гоа! & Porter 16412 (М‹ )), Croat 38120 (HUA, INB,
vi UB, VEN), Croat & Porter 16375 (MO); Chiriquí
Grande-Fortuna, 7.7 mi. S of Chiriquí Grande, 1.5 m W
of Punta Peña, Cr roat & Grayum 60116 (MO), Akers da
(MO); IRHE vic. Carras quilla & Mendoza 1239 (M
PMA); Almirante- -Ojo de nee 3-6 km W of ханын
РМА); е 10 mi. W of Ver
border, McPherson 11. 401 (CM, МО); Valle del Silencic 10,
along Rio Changuinola, ca. 1 km above mouth of Rfo Ter-
ibe, vic. Teribe ie population, Croat & Zhu 76422
(INB, MO, WU); Cocoa Cay, vic. of Chiriquí Lagoon, von
Wedel 2892 (F); Río Teribe vic. Teribe H, IRHE, Carras-
~~ 2005 (PMA); Changuinola-Tuibe Rivers, Zigla Rd.,
izor et al. 2578 (MO); limit trail of Par. Intl. La Amistad,
from 175 brada Boca Chica to Quebrada 8 Polanco
1591 (PMA). Chiriqui: Fortuna Lake Area, 3.4 km N of
Quebrada Chorro, 1.6 mi. N of center of bridge over lake,
Croat 74958 (MO); vic. Fortuna Dam, McPherson 9829
(MO); Quebrada Los Chorros-Quebrada Hondo, N of For-
tuna Lake, Churchill & Churchill 6105 (MO); Fortuna-
Chiriquí Grande, 0.7 mi. NW of center of dam, Croat
Zhu 76482 (INB, MO, PMA); trail from rd. near Колу
Nursery to Río Hornito, Thompson 5028 (CM). Coclé:
Cont. Divide, N of Penonome on rd. to Coc lesito, Hammel
4049 (MO). Mm Santa Rita Ridge rd., mi. E of
Transisthmian Hw hers Merello 6 (MO);
Santa Rita Ridge R d., ca alk from end of rd.,
Antonio 4488 (MO); a Rs Ridge Rd., ў
ie Roosevelt Hwy., Croat & Zhu 76942 (CR, GOET,
GUAT, HUA, INPA, ISC, LE, M A TEFH, UB,
WISC 3 Puerto Pilón- е lo, ja Соп he, ca. 1.5 mi.
8 of rd., Croat & Zhu 76254 A); Río Guanche,
3—5 km above bridge, dem 79348 (B, INB, MEXU, MO
US), ud us М 0); 3-7 km above bridge, Hammel
et al. ; са. З s ory bridge, Croat 49761
ы Еу 8 на arra Lloro Galdames et al. 1138
; Río poe 97 7 40768 (MO). Darién: W side
Pirre, Cre 4 (MO); Río Tuquesa, ca. 2 km
air distance from 18 0 it. d le, near upper ee 9
5 27161 (MO); Serranía de

cucha Ruido, above Cana Gold

Croat 38229 (Е, MO

—

. Croat 67379A

(MO). § Blas: Comarca de Kunayala, a El
е ai Rd., 10.1 mi. N of Inter-am. Hwy., then 5
0.5 mi. N Paseo Mariska, Croat & Zhu 77023 (MO): S

of Pue arto Obaldía, Croat 16769A (MO); trail s doc я а
airport to village of Cangandf, de Nevers et al. 7407 (MO,

A); El Llano—Cartf Rd. km 16.7, trail W to же, 5
km from rd., de Nevers & S. Charnley 5898 (MO, PMA);
Canagangí, de Nevers et al. 5727 (MO). Veraguas: Boca
de Concepción, in Golfo de los Mosquitos, McPherson
11381 (MO). COLOMBIA. Antioquia: Mutatá, Corr. Lon-
gani, Callejas et al. 5661 (HUA). Chocó: trail from Río
Mecana to Alto de Mecana, Gentry & Juncosa 41037
(MO); Serranía de Baudo, Las Animas-Pato, Río Pato, 10

km SW of Pato, Croat 56070 (CHOCO, MO); = wae
Rfo San a Killip 35113 (COL, US); Alto de 5. Gen-
try & Forero 7342 (COL, MO); Bahia Solano, ^in erto Mu-
lis, Gentry & Forero 7217 (COL, MO); Bahia Som, Croat
57462 (CHOCO, COL, MO); N of ш Solano, Cerro
Mecana, Juncosa 1795 (МО);
quita, Juncosa 1898 (MO),

Noanama, Forero et al. 4571 (C OLX Río Bic pr hpc
of Río San Juan, Noanama, Forero et al. 9 (COL);
Acandí, Quebrada Sardí, El Páramo, rius et a 1199
HUA, MO); Corr. San Francisco, Vereda py sitio
El Páramo, Que Байа Zardí, Betancur et al. 1177 (HUA);
Vereda Coquital, Fonnegra et al. 2899 (H е a 2907
HUA, NY); Nuquí, 5 Arusf, vic. of Arusf,
Est. des El Amargal, Croat & Mora 8 83652 ( е 270)
MO); Corr. Arusí, E iol.. El Amargal, Mora 170
Se "ECUADOR. Esmeraldas: Zapallo Grande, Río
Cayapa, Barfod et al. a 348 (AAU); Lita-San Lorenzo Rd.,

0.9 km E of El Durango, 19.8 km W of Alto Tambo, Croat
et al. 82520 (MO); Playa de Oro, 1 km from Río Santiago,
Cerón & J. Corozo 33858 (QAP), 33947 (QAP), Cerón &
J. Corozo 34097 (QAP); San Lorenzo-Mataje, departing
main Lita-San Lorenzo Hwy., 11.6 km N of Gasolinera
San Lorenzo, 2.9 km W of main Lita-San Lorenzo Hwy.,

Croat et ۳ 84041 (AAU, B, CAS, COL, DUKE, (
MO, NY, P, UB, US, WU); Cotacachi Cayapas,

10 05 Rio 1 Sector Loma Linda, Tipaz et al. 2280
(MO, QCNE); Río Cayapa, Zapallo Grande. lia et 95
48154 (AAU, MO); Zapallo Grande, Kvist

(AAU, QCA); Rio Cayapa, Zapallo Grande, *
40756 (AAU); Rio Grande, at Zapallo Grande, Barfod &
Skov 60101 (AAU); Rfo San Miguel, upstream from Pueb-
lo Cayapas, Holm-Nielsen et al. 25355 (AAU); San Lor-
enzo, Sparre 18326 (S). Morona-Santiago: Santiago-Mo-
rona, Río Morona, 23.4 km E of Santiago, Croat 87448
(MO, QCNE).

~=
c
2
E
E

©
=

8 8
8

— —

19. Dieffenbachia obscurinervia Croat, sp.
nov. TYPE: Panama. San Blas: trail from dock
to airport to village of Cangandí, 9?24'N,
79°24’ W, 3-30 m, 26 Mar. 1986, С. de Nevers,
Н. Herrera & 5. Charnley 7409 (holotype, MO-
3475792!; isotypes, Bl. US!). Figures 19, 29А.

Planta 0.8—1.5 m; internodia brevia, (1)3—4(5) em lon-
ga, 1.5-2.5(3) em diam.; pe 'liolus 8-12 em longus, vagin-
atus ad medium vel ad apicem; lamina anguste elliptica,

illam; pedunculus (1.7)3—5 em longus; spatha 11.5-20 cm
longa; spadix 10-18 em longa, cum parte pistillata 5—5.5
cm longa.

Slender herb, 0.8-1.5 m tall, stem decumbent on
older parts, weakly rooted, leaf scars inconspicu-
glossy, (1)3-4(5) em long, 1.5—

2.5(3) em diam., dark green, epidermis fissured mi-

ous; internodes

nutely into a netlike reticulum becoming uniformly
fissured and brown-scurfy with age; petioles 8-12
em long, averaging 10.6 cm long, sheathing % to
throughout (average 0.8 their length), light green or
yellow-green with the surface dark green-splotched
or dark green with white or yellow spots (sometimes
with spots forming a repeated series of irregular

Volume 91, Number 4 Croat
Revision of Dieffenbachia

2004

A

ite Wd

6mm
ese

—A. Cluster of several potted plants with plant on
's and inflorescence

== D. Close-up of

Dieffenbachia obscurinervia. A, B. (Croat 12660).
left with open шан scent (NS Close-up of crown of plant showing adaxial and abaxial surface
at anthesis. —C. Close-up wm n showing mottled epidermis and speckled petioles (Croat 61234).
inflorescence d Es both Dna and staminate portions of spadix (Croat 13849).

Figure 19.

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bands); sheath 6.7-10 cm long, the tip usually
rounded to inequilaterally emarginate, rarely de-
current, frequently with one side emarginate and
with the other side acute; unsheathed portion lack-
ing or to 5.2 cm long, sharply to bluntly sulcate;
blades narrowly elliptic, 20-30 cm long (averaging
24 cm long), 5-8 em wide (averaging 7.5 cm wide).
2.4—5.2 times longer than wide,
ger than petiole, slightly inequilateral, one side

1.6-3.1 times lon-

0.7-1 em wider than the other side, subcoriaceous,
weakly bicolorous, gradually acuminate, briefly apic-
ulate at apex, frequently somewhat falcate, cuneate

obtuse or rounded, often weakly inequilateral,
rarely weakly subcordate at base; upper surface dark
green, semiglossy, drying dark yellow-green to dark
olive-green; lower surface slightly to moderately pal-
er, drying yellow-green; midrib slightly raised to flat
above, concolorous, drying concolorous above. con-
vex to narrowly rounded below, dark green, densely
pale yellowish green-spotted, drying paler than sur-

—

ace or darker than surface below; primary lateral
veins 10 to 13 per side, weakly etched above, weak-
ly raised or not at all raised below; the interprimary
veins almost as conspicuous as primary lateral
veins; minor veins moderately distinct below. IN-
FLORESCENCES 1)3-
5 em long, somewhat flattened in cross section:
spathe 11.5-20 cm long, 3.2-9.5
pale green throughout,

—

l to 3 per axil; peduncle (1

times longer than
peduncle, dark green or
caudate-acuminate, sometimes sharply reflexed be-
low apex: spadix 10-18 cm long; free portion 5—9
em long; pistillate portion 5-5.5 cm long; sterile
segment less than | cm long. 6 mm diam., with
scattered staminodia throughout; pistils 20 to 40,
2-2.0 mm
stigma depressed-globose, 2 mm diam.; sta-
1.5-2(3.4) mm

long, flattened, oblong to clavate, grooved medially,

moderately closely spaced, scattered,
diam.;
minodia white, usually 3 per pistil,
drying flattened, thickened at apex; synandria ir-
regularly rounded with margins undulate, minutely
warty, widely sunken at apex, 1.8-2.6 mm diam.,
dark yellow-brown, matte on drying. INFRUC-
TESCENCE broadly arching: spathe mostly decid-
uous; spadix to 8 em long; berries red, broadly el-
lipsoid, to 1.5 em long, less than 1 cm diam.

Abior (Kuna) (de Nevers et al.

Common name.
0

Distribution and habitat. Dieffenbachia obscu-

rinervia ranges from central Panama (as far west as

Coclé) to northern Colombia (Antioquia and Chocó)
from 30 to 800 m in Tropical moist forest (T-mf) and
Tropical wet forest (T-wf) life zones (Holdridge,
1967)
Phenolog y.
er from May to December and fruiting collections

The species has been seen in flow-

have been reported from from September to May.

Discussion. Dieffenbachia obscurinervia is char-
acterized by its scurfy brown internodes, conspic-
uously splotched petioles, and narrow blades with
weakly developed primary lateral veins. It is not
easily confused with any other species but was in-
correctly called D. pittieri, a species considered re-
stricted to the Isthmus of Panama, for many years.
See that species for a discussion of the differences.

Paratypes. PANAMA. Canal Area: Pipeline Rd., mi.
1-3, N of Gamboa, 5. Knapp 1042 (MO); Pipeline Rd. at
Rio Agua Salud, Croat 12352A (MO); Barro Colorado Is-
land, Armour Trail 1280, Croat 8623 (MO
1000, Croat 12660 (MO); Drayton 1910, Croat 6775 (MO,
^ \ 1490, Croat 5759 (MO). Coclé: vic. El
Valle de Antón, La Mesa, Finca Macare nita, Croat ¢ Zhu

Portobelo-Nombre de

5 4484 (MO);
Di 1.2 mi. beyond jet. of rd. to Isla Grande, Croat
49791 (MO. TM. A): Río Guanche, ca. 5 km upstream from
rd. to Portobelo, паи & Trainer 14786 (MO);
de la Gloria,
. Panama: Balb ya West, Zapata et al. 2 1
ue trail off Llano-Cartí Rd., 4.6 mi. from jet. with Pan-
Am. Hwy., McPherson & Merello 8143 (MO). San em
Rio Cangandí, Cangandí, Н. Herrera 245 (MO, PMA);
sigandf, along El Llano—Cartf Rd., 0.7 km beyond Cuna
headquarters, 11.6 km from Pan-Am. Hwy., Croat 75149
(K. MO). COLOMBIA. Antioquia: Río Anorí valley, near
Planta Providencia, Shepherd 438 (MO, WIS); Anorí, Corr.
Prov., Soejarto & Renteria 3556 (HU. A); arar Río An-
a Quebrada La Tirana-Río Anorí, 2 km N of Quebrada
La buo 3 km upriver from Planta аен ча, Alverson

==
35

et al. 263 (COL); Carepa, Tulenapa Reserva (ICA), Turbo-
Mutatá, d km 5 of Turbo, Callejas et al. 4873 (MO, 2

Chocó: Nuquí, Quebrada Chaquí. Galeano et al. 4825
(MO); Quibdó, La Concepción, 15 km E of Quibdó, ic ins

2215 (US); Cordoba, Tierralta, Río Esme raldas-Rio Simí,

2 km above confluence. Bernal et al. 1158 (COL).

20. Dieffenbachia oerstedii Schott, Oesterr.
Bot. Z. 8: 179. 1858. TYPE: Guatemala. Agua-
cate, А. S. Oersted s.n. (holotype, С). Figures
20, 29A

Herb, 30-75(100) em tall (usually less than 50
cm): stem erect or partially reclining. often con-
spicuously clustered with numerous plants; sap

>
e 20. Dieffenbachia oerstedii. —A. Potted plant with inflorescences and gebe with mottled blades (Croat
68449). —h. Potted flowering plant with pale midribs (Croat & Zhu 76794). —C. Leaves and post-anthesis inflores-

cence showing ovate-lanceolate blades with scarcely sunken primary lateral veins (Cr гоа! 632084).

—Jp. Close-up of

Volume 91, Number 4 Croat
2004

Revision of Dieffenbachia

Figure 20. (Continued) stems showing p free-ending petiole sheath (Croat 36297). E. F. (Croat 68449). —
К plant with open inflorescences. —F. Close-up of flowering plant showing open spathe blade and exposed
staminate portion of inflorescenc

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moderately foul; leaf scars conspicuous, transverse
or oblique (when oblique, up to 2X as wide on one
side as the other), forming a T or forming a W on
open side of sheath; internodes semiglossy to glossy,
weakly warty on magnification, 1-5.7 em long, 0.8—
2(3) em diam., dark olive-green to blackish green,
medium green or dark green, sometimes variegated
with streaks of paler green, drying dark brown to
dark

20(30) ст long. (averaging 13.7 em long), 3—4 mm

yellow-brown, glossy. smooth; petioles 10—

diam., sheathing % to 34 (rarely nearly throughout)
their length (averaging 0.7 their length), medium
green, matte, sometimes finely streaked throughout
with darker green, usually weakly glossy and white
near base: sheath 2.5-21.5 em long (averaging 9.3
cm long), pale green to white on lowermost clasping
darker

stem), with margins involute, the tip with one side

portion (contrasting sharply with much
erect, free-ending and rounded to auriculate, with
the other side rounded to acute (sometimes not free-
Panama):

ending in Coclé Province, unsheathed

portion 5-13 em long. C-shaped U-shaped
cross section, convex adaxially, acute to bluntly an-
gled on margins: blades ovate to narrowly ovate or

(5.5)14—
(averaging 20.1 X

ovate-lanceolate or rarely oblanceolate.
22(35) х (1.7)4-14(21.5) cm,
8.5 em), l.
2.5 times longer than wide).

1—5.9 times longer than wide (averaging
e e D
0.8-2

(averaging 1.5). often inequilateral.

.4 times longer
than petiole
somewhat thinly coriaceous to subcoriaceous, mod-
erately bicolorous, gradually acuminate and apic-
ulate at apex (the acumen 5 mm long), acute and
weakly decurrent to obtuse or more often rounded,
sometimes subcordate at base; upper surface matte
and subvelvety to weakly glossy, dark green, fre-
quently splotched light or medium green or with
white areas especially near midrib (all variations
frequently found in a single population). drying
dark brown to gray-green, concolorous, sometimes
faintly dark-striate; lower surface matte to weakly
glossy (epidermal cells raised and sometimes trans-
lucent), drying yellow-green to yellow-brown, some-
times faintly dark-striate, slightly paler: midrib flat-
raised to obtusely flat-raised above, concolorous or
sometimes white above (sometimes mottled on
plants with mottled leaves, sometimes faintly dark-
striate on both surfaces), slightly paler and convex
to broadly convex to bluntly acute below; primary
lateral veins (4)6 to 9(11) per side, departing midrib
at a 40°-45° angle, broadly arcuate-ascending,
sunken to quilted-sunken above, slightly darker
than surface, weakly convex-pleated below; inter-
primary veins weak or as conspicuous as primary
lateral veins; minor veins indistinct above, moder-

ately distinct to moderately obscure below: “cross-

sometimes visible. INFLORESCENCES 1 to
2 sometimes 3, rarely 4 per axil: peduncle (2.2)3.5—

veins’

12(22) em long (average 7.6 cm long). И, as long
as spathe to fully as long as the spathe, averaging
0.43 as long. 6-13 mm diam., 2—4 mm diam. on
drying, somewhat flattened in cross section; spathe
(7.5)10-17(25.5) cm long. weakly constricted above
tube, medium green on both surfaces, sometimes
tinged whitish on back throughout (the median rib
green), weakly glossy to semiglossy outside, glossy
on inside, narrowly acuminate at apex: tube to 2—
i i to 8

cm wide when flattened; spathe blade to 2.5 cm

2.8 cm wide, 1.5-2.3 em thick when furled.

diam. when furled, 3.0-8 em wide at anthesis: spa-
dix (7)10-17(21) em long (averaging 14.6 em), 1—
5 em shorter than spathe: pistillate portion 4.3—
7.9(10) em long (averaging 6.4 em long). 5-10 mm
diam.: fertile staminate portion 3-8.5 em long (av-
eraging 5.3 em long). 5-7 mm diam., broadest at
middle, tapering toward both ends, especially at
bluntly pointed apex; mostly sterile intermediate
(dried),

with a few widely scattered sterile staminate flowers

segment (1)2—3.2 em long, to 2.5 mm diam.
in upper % and a few pistillate flowers in lower М,
sometimes with only sterile staminate flowers scat-
tered throughout, rarely almost bare: pistils (26)33—
46(54). moderately closely spaced except in the
lower 1.5 em and the upper | em (the distance
twice their

between them generally equaling or

width), up to 4 in a row across the width of the
spadix, subglobose, 1.5 X 1.4-2.6 mm; stigma de-
pressed-globose. yellow, 1 mm wide, puberulent;
style caviform with a weak central dome; stamino-

2—3(4.5) mm

—3 times longer than

dia clavate, white, drying orange.

long, 1-2 mm wide at apex, 2
pistil, usually weakly fused at base, sometimes well
separated, weakly flattened, thickened toward apex:
synandria 3 to 5 per spiral, 1.4-2.0 mm diam., the
margins smooth to irregularly and smoothly in-
dented, smooth and subrounded at apex. INFRUC-
TESCENCE to 22 em long: spathe orange outside;
berries bright red, globose, with 13 to 43 per spadix,
4—6 mm diam.

Distribution and habitat. Dieffenbachia oerste-
dii ranges from Mexico (Veracruz, Oaxaca, Chiapas,
and Tabasco) mostly along the Caribbean slope in
Central America in Guatemala, Honduras, Nicara-
gua, and Costa Rica (where it occurs on both
slopes) and west-central Panama. The species also
occurs on the Pacific slope of El Salvador (Depart-
ment of Ahuachapán). The species ranges from sea
level to 1260 m in Tropical dry (T-df), Tropical moist
(T-mf), Tropical wet (T-wf), Premontane wet (P-wf),

Volume 91, Number 4
2004

Croat 739
Revision of Dieffenbachia

and Premontane rain forest (P-rf) life zones (Hold-
ridge, 1967)
Phenology. Flowering of D. oerstedii occurs
throughout the year, but with the heaviest flowering
at the end of the dry season and the first part of
the rainy season, April to September. Fruit matu-
ration is more regularly scattered throughout the
year.
Discussion. This species is characterized by its
small stature (generally less than 1 m tall); fre-
quently clustered stems; and sharply C-shaped pet-
ioles that are whitish at the base and sheathed
mostly 4—% their length, with the sheath obscurely
free-ending and inequilateral with at least one side
usually merely rounded or acute rather than auric-
ulate. Also characteristic are the moderately thin,
usually small, + ovate-lanceolate blades, which are
generally acute to rounded or truncate basally and
matte or only weakly glossy adaxially.
Dieffenbachia oerstedii is the most widespread
and ecologically variable species in Central Amer-
ica. It is extremely malleable in terms of leaf size,
leaf blade shape, and markings, with different
blade coloration types (cf. Fig. 20A, B) all found
within the same population. For example, in pop-
ulations at Río Grande de Taracoles at Carara in
zosta Rica (0-200 m), the plants of this species
are robust. The populations of D. oerstedii at 1400
m in Braulio Carillo National Park (also Costa Rica)
have small and delicate leaves. In Costa Rica, the
leaf blades tend to be matte or only weakly glossy
on the upper surface. However, elsewhere in Cen-

„>

tral America the blades are often more glossy. .
collection from El Salvador (Selby 77-3078) has
blades that are initially rather glossy on the upper
surface and weakly glossy on the lower surface (al-
beit soon turning only weakly glossy above). Plants
in Panama and Costa Rica have blades 2—11 cm
wide and acute to rounded at the base, whereas in
other parts of Central America from Nicaragua to
Mexico the blades are often 14—18 em wide with
subcordate leaf bases.

Standley (1937) considered Dieffenbachia leopol-
dii (Bull. Catal. 1878) similar to or synonymous with
D. oerstedii, but the type specimen indicates that it
was actually collected in Colombia, where D. oerste-
dii does not range. The species is actually closer to
D. killipii (see discussion under D. killipii).

Collections from Mexico and Belize are larger on
average than those in Panama, Costa Rica, and
Nicaragua, with blades 16.5-35 cm long and 6-
16.5 cm wide (averaging 23 X 11 cm). Petioles for
the same area range from 8.5 to 30 em long, about
as long as the blades to 1.7 times longer than the
7.5 to 21.5 cm long,

blade with the sheath from

averaging 14 cm long (sheathed 0.48—0.9 the pet-
iole length). In contrast, plants from Heredia Prov-
ince in Costa Rica are smaller than average with
blades averaging 13.9 cm long and 5 ст wide (2.9
times longer than wide).

The distribution of Dieffenbachia oerstedii in Pan-
ama is apparently disjunct with some collections
known from far western Panama, but the species also
occurs in the vicinity of El Copé and La Mesa in
Coclé Province. The populations in El Copé have
cm long), but differ
only slightly from those in Costa Rica. The El Copé

somewhat smaller leaves (9.5-15

material is otherwise morphologically identical to
populations of D. oerstedii such as those found at La
Selva in northern Costa ;

The petiole sheath of iba Coclé populations is
merely rounded on one side and acute on the other
(vs. auriculate on one side and rounded on the oth-
er side for typical material of D. oerstedii). In ad-
dition, the midrib is not faintly striate on both sur-
faces as is usually the case with typical D. oerstedii.
The petiole scars are much more oblique than usual
with the internodes longer on one side of the stem
than on the other (vs. more nearly perpendicular to
the stem with the internodes of equal width on both
sides of the stem for typical D. oerstedii). Despite
the strong morphological similarities, plants from
Coclé Province, Panama, differ markedly in their
ecological requirements. Cultivated plants, for ex-
ample. will survive well only in an area of nearly
100% humidity. Alternatively, the Costa Rican ma-
terial from Heredia does very well in the drier parts
of the greenhouse.

In Mexico, Dieffenbachia oerstedii may be con-
fused with D.
leaf blades. Living material of the latter is easily

wendlandii since they have similar

separated in having petioles with the free portion
terete or obtusely and weakly sulcate (vs. sharply
C-shaped and sulcate in D. oerstedii), the base solid
green, and in having the sheath decurrent at the
apex with one margin overlapping the other (vs.
with both
sides visible and often protruded at apex and the

rolled in from both sides in D. oerstedii,

sides inequilaterally rounded to auriculate). Com-
pared with D. oerstedii, D. wendlandii is typically
a larger plant with longer stems, thicker internodes,
and larger leaves up to 33 cm long and 9.5-15 cm
wide, and with the midrib 1.2-1.4 em wide (vs. 5—
6 mm wide for D. oerstedii). In addition, D. wen-
dlandii has the stigma bowl-shaped at anthesis with
a protruded central dome. In contrast, the stigma
of D. oerstedii is cushion-shaped.

Dieffenbachia oerstedii is similar to D. killipii in
general blade shape and size as well as in often
having the “flat-raised” upper midrib, but D. killipii

740

Annals of the
Missouri Botanical Garden

often differs in having petioles not at all whitish at
the base, blades which are typically semiglossy
matte and subvelvety to weakly glossy in D. oerste-
dii), and especially in having the spadix with the

—

VS.

pistillate and staminate portions nearly contiguous
rather than well separated.

Herbarium material of Dieffenbachia oerstedii
may be confused with D. the West
Indies. Both species sometimes have blades of sim-

seguine from

ilar shape, and both have petioles that аге com-
parably sheathed and sharply C-shaped on the free
portion. The two species differ in stature, with D.
oerstedii being much smaller and with blades matte.
often subvelvety, whereas those of D. seguine are at
a minimum weakly glossy on the upper surface. The
auricles on the free-ending sheath of D. seguine are
both rounded at the apex, whereas in D. oerstedii
one of the sides of the sheath is almost rounded at
apex and the other is usually acute at apex. How-
ever, the sheaths that subtend inflorescences in D.
oerstedii may have the apex auriculate on both
sides.

The type locality of Dieffenbachia oerstedii col-
lected by Oersted remains in doubt but it may be
from Guatemala. The type specimen contains only
the name “Sanguinillo” on the label. Also penciled
on the label is the name “Aguacato,” perhaps add-
Engler (1915:
“Schottige Berwülder

ed at a later date. 15) cited a col-
lection made by Oersted from
des Berges Aguacate” (perhaps Cerro Aguacate in
Sierra de las Minas). He also listed “sanquinello”
(Engler, 1915:
stedii (note the difference in spelling from that orig-

15) as a common name for D. oer-

inal label).

It is possible that Dieffenbachia oerstedii occurs
in the Lesser Antilles and in French Guiana. How-
ard 11744, purportedly collected along the road be-
tween Rousseau and Sulfur Spring on Dominica,
appears to be this species. Another specimen col-
lected in. French. Guiana (Croat. 74319) along the
Cayenne—Regina highway, as well as cultivated ma-
terial going by the name “D. oerstedii variegata"
(Lyon 67-1086), appears to also represent this spe-
The same taxon is in cultivation in Port-au-
Prince, Martinique (perhaps originating from
French Guiana). Since the species is not apparently

cles.

widespread in the areas mentioned, the field-col-
lected plants may in fact be plants escaped from
cultivation, Living specimens studied of the mate-
rial from French Guiana and the cultivated material
from the Lyon Arboretum are characterized by hav-
ing the midrib creamy white from the lower М to
the upper М of the blade. A similar feature is found
in some populations of D. oerstedii in Costa Rica.

Additional spec ime ns
‚ Mo

seen. BELIZE. El Dorado,
CE 306 (F, GH, ).

; Caves Branch, halfway

. Herman's idi W Биер! 1176 E M. МО); Cayo,
"dide Creek Districts, Hummingbird . betw. mi. 25—
34, Dwyer & Dieckman 13008 (MO); Vaca сасы Vaca

Falls, Balick et m 2080 (MO): Stann Creek, Coc E
Basin, Jaguar Pres., 10 km W of Maya Center, off 5 Hw
Balick et al. 2716 (MO): Toledo, vic. of trail to Espe ranza
beginning 1 mi. N of Columbia Forest Station, Vanderveen
MO): Columbia For. Stat., Dwyer 9920 (MO); San
José trail to Esperanza 1 mi. N ids aW Forest Station,
Croat 24250 (MO); vr е 6.7 mi. N of Columbia Forest
Station, Dwyer 1118: Bl: ak n. "Ric hardson Creek, af-
fluent of Bladen с. i е part of Maya Mountains,
Davidse & Brant 31879 (MO); along Bladen Branch from
Ric Pup Cree : 8 Quebrada de Oro, staan & Brant
32366 (MEXU, ; Bladen, Solomon Ca vic. of the
jet. of Ric ж е reek and Bladen Branc de foothills of
the Maya Mountains, Davidse & ass 32410 (MEXU,
MO): Bladen, Bladen Nature Reserve, ca. 2 air km N of
upper Bladen Branch, Davidse 35802 (ВАН, MO, SEL):
Bladen Res., Ek Xux archaeological site, Davidse & Holst
36041 (MO, MY y: upper Bladen Branch basin, along main
Bladen Canyon, Davidse & Holland 36505 (BRH, MO):
Columbia Res. near Crique Negro, Whitefoord 3284 (BR,
MO). COSTA RICA. Alajuela: Laguna Hule, NE of Cerro
Congo, Luteyn 3342 (DUKE), Schubert & Rogerson 619
(A); canyon of Rio СЫ and W slope and summit
‹ ridge be tween Río Cariblanco and Quebrada Quicuyal,
. Grayum et al. 6194 (MO); 3 km N of
La Luisa and 15 de N of Grecia, Murphy & Jacobs 1289
E San Carlos, Haber & Hammel 1799 (МО);
Cordillera de Tilarán, San Ramón-Bajo Rodríguez, vic. La
1 0 8.9 mi. NW of center of San Ramón, Croat 68069
(CR, К, MO): 10 km N of Bijagua, Croat 36473 (DUKE,
F, D MO): Ораја, Brasilia 1.5 km 5 5 town, Finca de
Mario Jirón, Herrera 1636 (INB, MO); 22 km NE of Que-
sada by air, 4 km W of Muelle San Carlos, Liesner 14102
07 22 id NE of Quesada by air, 4 nm W of Muelle
San Carlos, Liesner 14155 (B. К. МО): 2 km N of Santa
Rosa, Liesner et al 15035 (B, MEXU,
1 80 0 5 Blanca, Finca Rio E gro.
О); rd. to Los Angeles, NW
m 3317 (DUKE); San йы Bajo Rodríguez, 12
km NS of Los Angelos, 16 km NW of San Ramón, Croat

szi

78830 (MO): vic. kn markers 11-12, ca. 7 km NW of Los
i los, 11-12 km NW of San 5 78859

pid 1000 5 de Tán

Dod. fp › (MO): Rio ns P йн of Volc an Mira-

valles, W of Bijagua, жай al. 3 (F, MEXU, MO):
San Carlos (Pital), de La Legua, Hammel 20231
(IN (В); Río Samen ie ‘la vo Aguilar 5204 (INB, МО);

San Ramón, ca. к о NW of San Ramón, و‎ 3263
(DUKE); along rd. from San Ramon, N of Balsa, ca. 8
km N of bridge Over Soa Volio, Stevens 13761 (MO):
3.5—4 mi. W of San Ramón, Croat 46785 (INB, MO); Río
Grande, San ено, Carvajal 273 (К. MO): Upala, 13.8
km N of Bijagua, Croat 36444 (MO); Upala Cantón, Est.
Biol. San Ramón, Dos Rios, Chinchilla 137 (INB. MO):
pala. Río Zapote, 4 km NNE of Bijagua, Croat 36297
(MO): 3.5 km W of Fortuna, 2.5 km NW of New Volcán
Arenal, Taylor & Taylor 11660 (MO). Cartago: slopes of

Miravalles above Bijagt ua, L. Gómez 19038 ( de Cantón
de Turrialba, 6 km f La Suiza on the rd. to Pa
Kennedy & Solomon 4629 (F, INB, MO).
SW slopes of Volcán Rincón de la Vieja and Volcán Santa

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

María, Burger & Pohl 7825 (F); La Tejona, N of Tilarán.
Standley & 1 46000 (U IS); PN Guanacaste Est. Men-
NBio 186 (INB. MO); Tilarán, San Pe-
dro de Río Chiqui, Monteverde, - & Bello 7191
(CR. МО); La Cruz-Santa Cecilia, Finca La Pazmompa.
Ríos et al 109 (CR); PN Rincón, Rivera 623 (K, MO): Las
Nubes de Río Chiquito 1 km NW of village on Cont. Di-
vide, Haber & Atwood 9163 (INB. MO): PN Guanacaste,
Est. Cacao, Carballo et al. 47 (MO); Cord. de Guanacaste,
Rincón de la Vieja, near refuge
Quebrada Grande. Barringer et al. 4061 (V. MO); PN
Guanacaste, Est. Mengo, Volcán Cacao, /NBio I 186 (CR):
Liberia, siguiendo el camino entre Nueva Zelandia (Que-
brada Grande) y Dos Rios, Upala, San Gabriel, C. Herrera
el al. 2 MO); Liberia, PN Rincón de la Vieja, Cor-
> о aste, sendero al Volcán, Taylor 216
(CAS, CR, INB, MO): Nandayure, Nicoya,
Bejuco, finca de Abel Rodríguez, A. Rodríguez & Estrada
142 (CR, INB, MO): а Standley K Valerio 45008
S); 7 ra de Tilarán, m Morenas.
Río San Lorenzo. 6. Rodrigues 32 (CR, . Heredia:
"2 a ield Station on Rio a rto. Vie) 3
just E of its jet. =ч a Sarapiquí, Jacobs 2159 (DUKE
Wilbur 37337 (DUKE), Wilbur 37243 (DUKE). Wilbur :
оч 34962 (DUKE). Folsom 8712 (DUKE), Hammel
5 (DUKE), MacDougal 1090 (DUKE), Wilbur 28249
(DUKE): area between Río Peje and Río Sardinalito, Atl.
slope of Voleán Barva, Grayum 6918 (MO): betw. Río Peje
and Río Sandinalite, Atl. slope of Voleán Barva, Grayum
6925 (MO); PN Braulio Carrillo, betw. Río Peje and head-
waters of Río Sardinal, Atl. slope of Volcán Barva. Grayum
G. Herrera 7829 (CR, МО); 8 km E of San Ramón,
Loiselle 119 (MO); La Selva or Zona Protectora, Croat
JA, К, MEXU, MICH, MO, К). Opler 246 (F):

Tirimbina, Proctor 32251 (Ы bs

go, Volcán Cacao,

Peninsula de

San Isidro, Valle Central.
Valerio 246 (CR). Puntar-
Norte-Panam p der, З km N of turnoff to
. Croat & D. Hannon 79199 an MO, US): ca.
17 km N of San Vito on rd. to Potrero Grande, Davidson
7164 (MO, RSA): betw. guard station & Quebrada Bonita.
Carara Res., Grayum & Warner 5710 (МО); Ref. Nac. Gol-
fito, along 5 tributary of Río Cañaza, upstream from cross-
ing of Golfito- Villa Briceño rd., Grayum 9251 (MO): Jardín
Boránion Wilson. W of Río Jaba. 1.5-2 km SW of Las
Cruces de Coto Brus, „бтауит 9277 (СК. MO):
Баш. Шай l mi. ' of Cañas Gordas, Croat 22252
(MO); Quebrada Bonita, to ca. 1 km E of Costanera hwy..
Carara Res., Grayum 4765 (MO); omg: short rd. to Golfito
from Villa Briceño on Inter-am. Hwy., V
ba, ca. 6 km from Golfito airport, Cal & Grayum 59929
(CR, MO, US); 9 km W of Monteverde on rd. to Inter-Am.
Hwy., Haber & Zuchowski 9251 ү INB, МО);

vado Sirena, Monkey Wood, 381 (CR.
КБ Rio San Luis river valley below community
on Pac. slope, Haber et al. 4979 (MO): San Luis, Montev-
erde Finca de Chepe Rojas, Bello et al. 42 (CR. 6. MBM,
MO): 8 km N of Baranca, | km N of MiraMar turnoff, W
side of km 123 on the Inter-Am. Hwy., Quebrada Negros,
Liesner et al. 15122 (CR, МО); foothills of the Cordillera
de Talamanca, vic. of Helechales, along the Río Guineal,
Davidse & Herrera 26262 (CR, MO); Pan-Am. Hwy. km

122, Hammel et al. 13962 (CR, MO, US): Cantón ч ат»
Rancho Quemado, Quesada 175 (CR, MO. R, UB.

hills N of Palmar Norte, along trail to Jalisco, Croat. a
(MO); Est A ues Bonita, Res. Carara, Croat 79072
(CAS, INB. MO): Orotina- dino. in valley of Río Grande

Tárcoles. | km S of Quebrada Ganado, woods behind Ho-

side of Fila Gam-

Kernan

ee sum along rd. NW of

tel Pink Paradise, near sea level, 5 km 5 of bridge over
Río Agujas on rd. to Jaco, Croat 79075 (INB, MO): Sector
Fila Gamba hills behind Esquinas Rain
Forest Lodge, along Quebrada Negra, at end of side rd.
off of on Bric ‘епа to Golfito Rd.. Croat & D. Hannon
1 (CAS, CM, COL, Е, MEX CU. MO, NY. SEL, ТЕХ,
N e Nicoya рашка, Curú. Sanders et al. 19322
120 Canton de Buenos Aires, Uj jarrás, headwaters of Río
Kuivé, trail to Olan, Chacón 364 (F. MO): Coto Brus, Osa
Peninsula, Sabanillas de Limonc ү, L. Gómez 22016 (CR,
MO); Golfito, Albergue Cerro de Oro, en el Sendero La
Tarde, Moraga 173 (CR, INB. чу PN Corcovado, Est
Sirena, Sendero Ollas, Picado & Gamboa 134 (INB, MO):
Quebrada Negra, Marten 831 (F), Aguilar 2412 (CR, INB.
MO. NY): Fila Costeña, اسا‎ C ruces, ; Handenberg of Río

Esquinas, vic.

(CR. INB У: ‚ Aguilar 2380 (INB.
MO): Río Sandalo: Dodge & Goerger 10157 (F); Cordillera
de Tilarán, Finca Buen а (Arco Iris), Monteverde,
Fuentes 367 (CR, INB i Finca el Gaucho, Ocampo
3411 (CR); Península M „ Est. San Miguel,
km S de Malpais. Fw My 7 el. 20114 (MO): Granadilla
s.n. (ENCB). San José: Río Chirripó

General Valley, Burger «e Liesner 7111 (V.
Río Hondura, Lent 2789 тА Montañas Ja-
NE of Bijagual de Turrubares. Carara
tes.. Grayum et al. 5862 (MO); Zona я La Can-
greja Forests along Río Negro, ca. 1.5 km E of Santa Rosa
de Puriscal, Grayum et al. 8345 (MO); Quebrada Micos,

са. &

Curridabat,
del Pacífico,
MO. PMA):

таса. ca. 3 km
|

са. 8.5 km of C 5 Colón, Grayum & Sleeper 6100
(MO): San José, Vale 1355 (F); Bijagua. I. Gómez

205624 (MO); Río vid Aguilar, жапе) 38942 (US):
ех Colón, Fine а El Rodeo, Nilsson & Manfredi 505 (F,
; Puriscal, Z а Cangreja, Cerros de Puriscal. Falda
б erro Cangreja, Santa Gertrudis, Cabeceras Rio Negro,
Morales et al. 5413 (INB, МО);
Braulio Carrillo Y Lye. Hwy.
Croat 78784. (INB, , NY. WU
achapán: i tae et ie 408 ( M.
intersection with rd. to Rio Cara Suc la. Croat 42133
. MO); Finca Colima, Sierra de Apaneca,
Standley 20085 (US); El Imposible, San Benito al N of
del Nacimiento del Río Aguachapio, Sandoval Chin-
= 352 (MO): La Libertad. Villacorta et al. 314 (LAGU,
. US): Finca Los Naranjc os, SW of Santa fo. 10
ip (F); San Vice 'e vic Standley 21414
(US). GU ATE MAL Alt ta Verapaz: Sierra de las Minas.
Quebrada Merce = S. Finca Mercedes,
E. Martinez et al. 22713 (MEXU, MO); Finca Mercedes.
Teleman, Panzós, E. Martínez et al. 23474 (MO): Río levo-
lay, N & NW of Fine a Cubilguitz to Quebrada Diablo,
Steyermark 14.75:
above Finca Montevideo, along Barranco m and
tributary of Río Pantaleón, Steyern y 5207t A MO
Chiquimula: Municipio Olopa, vic.
(M). Escuintla: Torolá, D. Smith 2
US); La Lindas, Standley 65041 (F); и Rio Jute
‚ Standley 63529 (Е). Standley 63620
n j: Torolá. . Guatemala:
Aurora, Aguilar 256 (F). Huehuetenango: Si
Cuchumatanes, Steyermark 49321 (F). Izabal: above Se-
lempim along rd. to Bocancha and base of Sierra de La
Minas. Fórther 10213 (M); Montaña del Mico, Ste :yermark
38775 (F); near Quiriguá, eie 72447 (Е); ca. 11
E of Santo Tomas, Croat 41655 (GUAT, MO); Selempim-
Bocancha, base of Sierra em 19 5 Minas,

10213 [232] (MO, MSB); Montana del Mico, Steyermark

SE

oe Z de ( 'oronado,

шанүй,

Telemán, Panzós,

Chimalte mango. Vo can Fue 280.

=
—
>

Finca la
erra de los

d

742

Annals of the
Missouri Botanical Garden

38647 (F). Jutiapa: vic. Jutiapa, Standley 75669 (F); be-
tween Mita and Asunción Mita, Steyermark 31763 (F). Pe-
tén: between Finca Yalpemech on Río San Diego and San
Diego on Río Cancuen, Steyermark 45410 (F). Quezal-
tenango: Retalhuleu, near Chivolandia along rd. to San
Felipe, Standley 87180 (F). Retalhuleu: Pueblo Nuevo,
р: 342 (US); Río Samalá, vic. San Felipe, Steyermark
55 (F). je пиш below Barranco Hondo, Stan-
de 88988 (F). San Marcos: 3 km SW of San Rafael Pie
de Cuesta, Harmon & Fue "ntes 4740 (MO); Río Chopal.
Finca El Porvenir, S-facit ng slopes of Volcán Tajumulco,
ves pilla 37456 (F); Steyermark
7153 (F); near El Molino, Standley 78523 (F); Río de
“ Esclavos valley, near El Molina, p 60715 (F);
Volcán Tecuamburro, Heyde & Lux 4654 (GH, K. NY, US).
Sololá: S-facing slopes of Volcán Аша, above Finca
Moca, Steye бани: 47908 (F). Sue pres FEE near Pueb-
lo Nuevo, Standley 66844 (V); near Las Lajas, Standley
58291 (F). HONDURAS. Coyol, Carleton 508 (US), Stan-
dley 26305 (F, GH, US). Atlantida: along rd. for munic-
ipal water supply of Tela, Lancetilla Botanical Gardens,
on rd. са. 2 mi. WSW of Tela and S of main hwy., Croat
& D. Hannon 64622 (MO, TEFH, US); Campamento Que-
brada Grande ca. 10 km SW of La Ceiba, base of N slope
of Pico Bonito, Liesner de Mejía 26236 (MO); 1
4 km S of Tela, Mena а (TEFH); sendero a la Pica a, El
Dorado, Cruz 354 (TEFH); ca. 3 mi. Tela, Webster et
al. 12624 (US), e et al. 12625 (F, MO, US); Tela,
valley above Exp. Stat., Mc 9 et al. 3193 (ENCB,
F, MO, NY), Mae Dougal et al. 3299 (Mí D Nec Tela, Pfei-
fer 2163 (US), Standley 52702 (F, US); 10 mi. SE of Tela
along Río Lancetilla, Croat 42645 ANB, MEXU, MO,
PMA, TEFH); Rfo San Alejo, S of San Alejo, Standley
7700 (F), La Ceiba area, 35 km S of La Ceiba on rd. to
Olanchito, Madison 712 (GH); La Ceiba, Mt. Cangrejal,
Mt. it jal, La Ceiba area, Yuncker et al. 8395 (F, GH,
K, MO, US). Comayagua: ca. 2 km S of Lake Yojoa,
Balick et al. 1738 (MO). сар 24 km E of Eds m
Harmon & Dwyer 4035 (MO, MEXU); Nueva d
mi. S, Harmon & Fuentes 6419 (MO). Graci к Шо:
ae Bila, 200 km cd of Puerto Lempira, Nelson & Cruz
5 (MO, TEFH, ОМО). Yoro: Cordillera eei de
Du. be S of San Jose de Texiguat, Davidse et al. :
(MO). M XIC CO. € /ampec ‘he: El Maculisal, 40 km Ae A
de la carretera, Escarciga, Chetumal, Bravo s.n. (MEX
30199) (ME XU . Chiapas: Chiapas, Cabrera et dl. 1
ке Izabal, ar Livingston, E. Martínez et t e 23175
SXU); 2 mi. S of Chiapas border along Hwy. 195, 8 mi.
N of Pichuc dea Croat 40087 (MO), Croat 40089 (MO);
60 mi. SE of Palenque, Croat 40163 (CHIP. MO); near
ruins at Palenque, Spellman et al. 164 (F, MO, NY); 2.5
mi. N of Isthuatan, Croat 47868 (MO); Bochil-Pichucalco.
17.1 km SW of Pichucalco, Croat 78678 (MO); 20 km S
of Palenque on rd. to Ocosingo, Mayo & Madison 301 (К);
Mpio. Ixhuatán, Clarke 60 (DS): Ococi 9100 19 km NW of
Crucero Corozal, E. Martínez 13445 (M . MO); Tene-
japa, along Río Tanate at. Habenal, paraje of Mahben-
chauk, Breedlove 12752 (F); Palenque Archaeological
Site, 3 mi. S of Palenque, Thorne & Lathrop 40559 (RSA);
Hío Cuxtepeques, near Fi
(DS); Las Margaritas, Breedlove & McClintock 34192 (DS):
Mapastepec, Río Testecapa, 10 km SE of Mapastepec,
(DS); Ocosingo. 5 km SW of
Santo Domingo, 120 km SE of Palenque on rd. to Bonam-
pak, Davidse et al. 20440 (CM, MEXU, MO); Ocosingo, 3
km NW of Vertice del Chixoy camino a Boca Lacantum,
E. Martínez S. 13630 (MEXU); Río Usumacinta, at ruins

T

of Yaxchilán, к 33839 (DS); ус. Song en ar-
ре al site, Davidse et al. 20326 (MEXU, МО); 6-
2 S of Palenque on rd. to Ocosingo, Breedlove 34977
(DS): Pie hucalco, cerca Campo Aviacion, F Miranda 7546
MEXU); Solusuchiapa, 2-4 km below Ixhuatan along
road to Pichucalco, Breedlove 24166 (DS). Oaxaca: Choa-
pan, Mpio., San Juan Lalana, trail Jalahui-Arroyo San Pe-
dro, Noriega & Н. Vasquez G. 1353a ( era Tabasco:
Cerro las Campanas, 3 km E of Teapa, ca. 50 km S of
Villahermosa, Conrad et al. 2863 (MO); vic. of Teapa, Tea-
pa-Tacotalpa, 3.1 m E of Teapa, Croat & D. Hannon
65370 (MEXU, МО); 3 km E of Teapa along rd. to Jalapa,
Croat 40107 (MO); Grutas ye Ocona near Teapa, Davidse
et al. 29516 (MEXU, MO); Тас ge a 3 km E of Lazaro
Cardenas, Cowan 2063 (MEXU, MO); Teapa, Cerro las
Campanas, 3 km E of Teapa, ca. 50 km S of Villahermosa,
Conrad & Conrad 2882 (MO). Veracruz: Cordova, Bour-
geau s.n. (P); Las Palmas-Catemaco, km 18, Leija & Garza
3341 (MEXU); Las Palmas-Catemaco, km 18, C-12-A,
González 3341 (MEXU); Las Cruces, Las Choapas, Gómez-
Pompa 1505 (F); Ebiotrolotu, Anaya 1 (MEXU); 6.5 km
from Santiago Tuxtla anc m on trail to fone del
Vigía, González 5597 (MEXU); Catemaco, 10 km N of Son-
tec шири. vic. Hotel Playa Escondida, ne 23733 (B,
GH, . MO, NY); E side of entrance of
MEN into the Gulf of Mexico, 7 i N
np Nee 22595 (F,

—

—

MO): Ce Md ta oc e near
Cate ie Hernández 542 (F, MEX ; Playa Es-
condi da. mi. airline NW of Sonceomapan Holstein

1 20425 (UC); ca. 8 mi. S of Catemaco near
5 on re d. to Acayucan, Moore Jr. & Bunting 8928
ВН); 5.7-6 Catemaco on rd. to San

2.6 n 8 of Los Tuxtlas Field Station, Croat 78695 (MO,
WU); 3 mi. SW of Sontecomapan, Los Tuxtlas, Barlow s.n.
(US); € te а, Рајар an, Tellez et al. 4466 (МЕХ); Co-
atzacoalcos, 6 mi. E of Coatzacoalcos, Hwy. 180, Croat
40062 (CM, MO, QCA, T ir : km SW
of Campamento La quos Nee 2996 XAL);
Hidalgotitlan, 1 km SE of Agustín Mean | Vee ` 297. 52
(MO); Río Soloxuchil, entre Hnos. Cedillo y T Escuadra,
M. Vasquez et al. V-907 (XALU); Las С hoapas. Las Cruces,
Nevling & Gémez- ре 1505 (F): Misantla, 8 km S of
Мау оп Hu to Xalapa, Madison 589 (GH, SEL); San
Andres Est. de Biol. Tropical Los Tuxtlas, N of
San D Tuxtla between Sontec و‎ and к
Croat & D. Hannon 63129 (MEXU, МО), 19 Aug. 1972,
1 627 (GH): San Andres 1 N and E fe of

puis Enc aiu 3 km NE of San Andres, Nee et al.
24759 (F, K. NY. SP. XAL), /barra 455 (MEXU),
Ibarra & С iG 180. 1 (MEX, MO, NY), /barra 645

(MEXU, MO), Dillon et al. 1837 (F, MO, NY), Cedillo T.
3645 (MEXU, MO), Calzada 338 (F, MEXU), Chazaro 416
XC): Monte Pío, 15 km al W de Catemaco, L. Gon-
du 1473 (ENCB, MEXU); Santiago Tuxtla, 6.5 km de
Santiago Tuxtla y 3.6 km camino al cerro del Мет Leija
& Garza 5597 (MEXU); Santiago Tuxtla, cerca Madero,
Ramamoorthy et al. 3763 (MEXU); 1 си. 5 152 SW.
of менш vic. Felipe E. Martínez, К. Robles G. 815
MEXU, XAL); Tlapacoyan, along Río a ‘team
from da nte de Tomata, 6 km SSW of Tlapac
al. 26103 (F, NY, XAL) PANAMA. Chiriquí: ı vic. Davia,
Pittier 2836 (MO); 13-20 km W of Río Chiriquí Viejo,
D'Arcy 10766 (MO): rd. to Río Serrano, Folsom et al. 2111

т)

—

e el

^

Volume 91, Number 4 Croat 743
Revision of Dieffenbachia

Figure 21. Dieffenbachia 5 —A. Habit of flowering plant (Croat 67526). —B. Potted plant showing ovate
Kade: 5 0 lirino n.). —C. Habit showing ovate-elliptic blades and inflorescences (Croat 74856). —D. Crown of plant

with blade showing quilted bun and close-up of open inflorescence (Croat 67526).

(MO); : W of Tolé, Río Cuvibora, Hammel 6264 (MO); Bur- 680-770 m. 25 Mar. 1993. T. B. Croat 7: jn }, 56
ica UE vic. of Puerto Armuelles, San Bartolo Lim-

> ‚| )- !: У У.
ite, 10-12 km W of Puerto essa npe Croat 22173 (MO). (holotype. МО-4342614'; i журе BI.

Coclé: 4—6 km N of El Copé, Montenegro & Chung 1462 COL!, DUKE!, Fl. GH!, INB! LI. Kl. MEX i

(PMA, STRI), Aranda et al. 2860 (PMA); La Mesa, N of NY!, PMA!, UB!, US!, VEN!). Figures 21,
El Valle de Antón, 2 km W E Cerro Pilón, Croat 37351 30A.
(MO). Veraguas: vic. Santa Fé, 1.7 eS past Escuela Alto
Piedra, Croat & Zhu 76859 (MO); 7 km 7 ^ school. EE i
° + Planta 0.75-2.5 m; internodia brevia, 3-4 cm diam.:
Nee 9912 ‹ :
Че alae Ls i & ۰ 1509 DUK li p 10-14 em longus, vaginatus + apicem: vagina
ultivated plan exico. Veracruz: Catemaco, culti- fsa- lanma ovata e (2@ E c frs
vated, prog 1692, Lankester Gardens, Cultivated, Kew (13.5 a 7-40 iar 3 ih per m Mir
70-76-494 (K); Finca La Selva, originally collected by He- ‘ ы | * „

cl 10-18 em longus; spatha 13—20 em longa: spadix
—18 em longa, cum parte pistillata 5-9 cm longa

len сареҳ 17 June 1971, Croat 68449 (CM, CR, MO ).

21. Dieffenbachia panamensis Croat, sp. nov. Stout erect. herb, 0.75-2.5 m tall: internodes
TYPE: Panama. Coclé: vic. of El Copé, 4.1 mi. short, typically more than twice as broad as long,

N of village, along old logging road which 1-3 ст long (typically somewhat longer on one side
leads down to the lowlands, 8°39'N, 80%36'W, than on the other), 3-4(5) em diam., dark green,

744

Annals of the
Missouri Botanical Garden

moderately glossy. LEAVES rosulate, erect-spread-
ing to spreading; petioles (0)10—14 cm long (aver-
aging 10.6 cm long), moderately erect, dark green
(white at base), sheathed throughout, the margins
flaring to recurled, sometimes incurled, markedly
crisped-undulate nearly throughout; blades ovate to
elliptic, (26)45-75 em long, (13.5)17-40 em wide
45.9 x 24.4 cm).
than wide (averaging 1.6 times longer than wide),

(averaging 1-2.4 times longer
markedly inequilateral (one side 2.5-5 em wider
than the other), obtuse to rounded at apex (the tip
inequilateral and weakly acute to acuminate), acute
to rounded at base, moderately coriaceous, mod-
erately bicolorous, dark green, matte and somewhat
velvety to glisteningly velvety above, weakly quilt-
ed and minutely wrinkled on upper surface, much
paler to moderately paler and slightly glossy to
drving dark. blackish brown to dark
yellowish brown above, vellowish brown to grayish

matte below,

brown below; midrib broadly convex or sometimes
flattened, 1.5-2 slightly paler. above.
somewhat more convex and slightly paler below:
primary lateral veins moderately quilted, (7)10 to

em wide,

20 per side, arising at an acute angle, then spread-
ing at 45°-00° angle, often at a somewhat wider
angle on one side, obtusely sunken above, convex
to obscurely raised and darker below; interprimary
veins usually | per pair of primary lateral veins,
about equal to primaries; minor veins not visible.
INFLORESCENCES 3 per axil; peduncles 10-18
em long (averaging 12.5 em long), somewhat flat-
tened, medium green, matte, weakly striate drying.
to 6-10 mm diam.: spathe 13-20 cm long (aver-
aging 18.4 em long), medium to pale green, weakly
and finely with darker,

striate on back surface,

oblique lines extending out to the margins, inner

surface slightly paler; spadix 12-18 cm long: free
part 8.5 em long; pistillate portion 5-9 X 1.8-2.2

ст, narrowed slightly toward the apex: sterile sta-

minate portion. 3—1.2 —].2 cm; mostly sterile

intermediate section 1.2 em long, with a few scat-
tered staminodia in the lower half; fertile staminate
pu: 5—7 em long, the flowers irregularly 5-sid-
ed, 2.5-3 mm diam.; pistils 3.5—4 mm diam.. ir-
regularly rounded at apex, closely packed, almost
contiguous; staminodia club-shaped, 4—5 mm long.
generally extending above the pistils, broadest at
base and apex, the tips 1.5-2 mm diam. Fruits or-
ange.

Distribution and habitat. Dieffenbachia pana-
mensis ranges principally along the Atlantic coast
of Panama from 50 to 850 m, on both slopes along
the Continental Divide east of the Canal Area.

Phenology. There are not enough collections of

this species to be certain of its flowering and fruit-
ing phenology. However, flowering collections have
been made in January, March, July, and September,
and fruiting collections during September and No-
vember.

Discussion. The species is recognized by its
fully sheathed petioles that are usually flaring to
recurled, by the moderately coriaceous, somewhat
velvety, weakly quilted blades, and usually broadly
convex midribs. It has up to three large inflores-
cences (mostly more than 30 cm long) per axil.

The species may be most closely related to D.
standleyi, which ranges from Nicaragua to Hondu-
ras along the Atlantic slope. Both share petioles
mostly fully sheathed, and have the sheath margins
rolled outward, but D. panamensis differs in having
blades more coriaceous, matte, and somewhat vel-
vely to glisteningly velvety above, weakly quilted
and minutely wrinkled on the upper surface.

Though the species does not occur in the same
area, it could be confused with D. horichii, a spe-
cies with a similarly fully sheathed petiole, but the
margins of which are incurled rather than flaring.
The blades of D. horichii dry mostly greenish rather
than somewhat blackened. Dieffenbachia horichii is
restricted to the Pacific slope of Costa Rica, ranging
from sea level to 900 m, while D. panamensis is
primarily known from the Atlantic slope of Panama
(also known from the Pacific slope at higher ele-
vations).

Paratypes. PANAMA, Coelé: Alto Calvario, 7 km №

of Copé, Folsom et al. 8264 (MO); Alto Calvario, old lum-
ber trail to Las Ricas, Limón & San Juan, Croat 68820
(MO): Alto Calvario Region, 4.5 mi. N of El Copé, 2.5 mi.
N of Escuela Barrigón, Croat 67526 (MO): 8 t above El
Copé, Hammel 778 (MO), Folsom & Collins 6486 (MO).
Tuquesa, ca. 2 air km from Cont. Div., vie.
of Kittredge gold mine, Croat 27206 (MO). Panamá:
above El Copé, 28 km NW of Penonomé, Read & Watson
84-75 (US)
22. Dieffenbachia pittieri Engl. & K. Krause,
IV. 23 De(Heft 64): 42. 1915
Panama. Canal Area [Colón]: Gamboa-
Las Cruces [currently Madden Forest Re-
serve], 50-80 m, 2 July 1911, H. E Pittier
3706 (holotype, US!: isotype, B not seen). Fig-
ures 22, 29B

Pflanzenr.

TYPE:

Herb, to probably less than 1 m tall; internodes
I-1.5 em long. 1.5-2 em diam., smooth, drying

dark yellow-brown with conspicuous pale petiole
scars; petioles 10-11 em long, fully sheathed, free-
ending and weakly auriculate on both sides at apex:
blades obliquely oblong, 17.8-20.5 cm long, 6-8.0

em wide, 2.9-3.1 times longer than wide. 1.8 times

Volume 91, Number 4 Croat 745
2004 Revision of Dieffenbachia

Jof Corm ЕЛ

-~

КҮҮМ
— EN

ж

UNITED STATES NATIONAL MUSEUM
DEPOSITED BY THE U.S. DEPARTMENT OF AGRICULTURE

\ PLANTS OF PANAMA

O бейс. ALI ope n

Canal Zone; altitud

* Along trail
€ \ ( 3 50 to 80 motors
2 3166
No. H. PITTIER, Collector July з, 1911

00088031

Figure 22. Dieffenbachia pittieri. Herbarium type specimen.

746

Annals of the
Missouri Botanical Garden

longer than petioles, shortly acute and markedly

inequilateral above, acute to obtuse at base; pri-
mary lateral veins 6 to 7
mostly in lower half of the blade, extending parallel
o the midrib, then spreading at 25°-30° angle,
nearly straight to weakly curved to the margin and
sweeping up along the margin, drying moderately

per side, concentrating

obscure above, convex and darker than surface be-
low; minor veins parallel with obscure and irregular
cross-veining on drying; surface drying matte, mod-
erately dark yellow-brown above, light brown and
finely pale-speckled below. INFLORESCENCES

3.5-5 em long, drying light

per axil; peduncles
brown, 2 mm diam.; spathe 17 em long, to 3.5 em
wide when flattened; spadix 14.5 em long: pistillate
portion of spadix to 8.5 cm long, 4 mm wide; sta-
minate portion of spadix 5 em long: mostly sterile
segment 2.2 cm long, drying 2 mm diam., with a
few scattered cup-like pistillodes throughout its
length; pistils 59, borne in a cup-like disk: stami-
nodia mostly missing.
Distribution and habitat. Dieffenbachia pittieri
is known only from the type in the Isthmus of Pan-
ama in an area of Tropical moist forest (T-mf) life
zone (Holdridge, 1967) at less than 200 m eleva-
tion. It is most unusual to encounter an endemic
species in this life zone, but the species is distinct
from other species in Dieffenbachia. There is a pos-
sibility that this could be a hybrid between D. kil-
lipii and D. isthmia because hybridization does oc-
cur in the
resemblance is with D. killipii, which also occurs

wild in Dieffenbachia. Its greatest
in this area and dries a similar color. Dieffenbachia
pittieri differs from D. killipii in having a dark
brown,
usually conspicuously ridged stems for D. killipii),

smooth-drying stem (light yellow-brown,

fully sheathed petioles (usually with the petiole
sheath ending well below the base of the blade for
D. killipii), blades with the midrib flat on the upper
surface (“square-raised” for D. killipii), and a spa-
dix with the pistillate and staminate portions widely
separated by a long, mostly sterile portion (vs. with
the pistillate and staminate portions more or less
contiguous in D. killipii).

Dieffenbachia pittieri has been confused with D.
obscurinervia (Standley, 1944; Croat, 1978), but it
proved to share little in common with that species
once the type specimen was examined. It differs
not scurfy

from that species in having smooth,
stems, unspotted, fully sheathed petioles, blades
with distinct primary lateral veins and with a mid-
rib flat,
with pistillate and staminate portions separated by

not "square-raised" above, and a spadix

a broad sterile segment rather than having them
contiguous or nearly so.

23. Dieffenbachia seguine (Jacq.) Schott, Wie-
ner Z. Kunst 1829(3): 803. 1829. Arum segui-
ne Jacq., Enum. Syst. РІ. 30. 1760.
guinum, orth. var. Aut жез (Jacq.)

Arum se-

ent., Mag. Encycl. 1801. Dieffenbac ^
plumiert Schott, ee rr. Bot. Wochenbl.
1852. TYPE: Plumier, Descr. Pl. Amer. n

61 (lectotype, designated here). Figures 23.
30B

Caladium maculatum Lodd., Bot. Cab. tab. 608. 1822.
Dieffenbachia maculata (Lodd.) G. Don, in Sweet,
Hort. Bri t. ed. 3, 632. 1839. Dieffenbachia maculata
eru Tic Halles 1 10: 145 13, nom. su
E YPE: Lodd., Bot. Cab. 1822 les

totype, i esignated here)

Пеј pete hia literata Schot ere Bot. Wochenbl. 68.

Dieffenbachia seguine fo. liturata (Schott)
Engl. Fl. 3(2): 175. 1878. Dieffenbachia se-
guine мы Qr (Schott) Engl., Bot. Jahrb.
Syst. 26: 568. 1899, Dieffenbachia Do var. li-
turata (Se p Engl., Pflanzenr. IV, 23 Dc(Heft 64):

47. 1915. TYPE: based on a cult ue id ‘tion

fide Se hot (not seen). Schott painting 1874. serves

as чы туре [microfiche 64. e 7] (lectotype, ги

tab. 608.

ле
Dieffenbachia lineata K. Koch & Bouché, Index Sem.
ek 14. 1853. dg cs seguine fo. lineata
"n & Bouché) Engl., Fl. Bras. 3(2): 175. 1878

Soa io se е ja hk ina (Schott) Engl.,
Bot. Jahrb. . 26: 569 5 se-
2 var. in irig (Sc shott) E ee Pflanzenr. IV, 23

De(Heft 64); 47. 1915. TYPE: New Granada, based
on a cultiv td г. at the
Garden, not seen. Schott illustration 1867 serves as
= Dre 1 һе 64 d 7] (lectotype, designated

he
Pieter m robusta Schott, Oesterr. Bot. Wochenbl. 65.
. Dieffenbachia seguine var. robusta (K. Koch)
97 Bot. J: hi rb. Syst. 26: 568. 1899. TYPE: Lo-
c ality unknown, cultivated collection of unknown or-
igin at Berlin Botanical Garden. Schott illustrations
1907—1908 serve as the m [microfiche 66 b2, b3]
(lectotype, designated her
Diefj m consobrina Se heit fu Aroid. 131. 1856.
YPE: Brazil. Rio Negro, Martius s.n. (holotype, M!).
bega n Schott, Syn. Aroid. 130. 1
1. Without loc ality, Poeppig s.n. (holot
W ed during 1 War 11); Schott Шашы
єч s e (microfiche 64. b 6) (lecto-

—

Ф

Syn. Aroid. 130. 1856.
iaibo, Martius s.n. e
& 184

pe, des

Diefenbach cognata : Schott
ҮРЕ: Suriname. Para

ч. [See also Schott ые иы 1845
шл: 77 Schott, Oesterr. Bot. 7 8: 387.
Venezuela. Without locality, Gollmer
s.n. ges vind B apparently lost); Schott. drawing
Sid (microfic 1 b. 7) serves as the type (lecto-
designate d here
hiec neglecta Se hott. Bonplandia 7: : 1859.
: Jamaica. Without locality, Distin ie

RU

Croat
Revision of Dieffenbachia

Volume 91, Number 4
2004

O Ame LE 2-80
2 AA а Д/

*

Figure 23. ас ie seguine. —A. Habit of plant showing the long creeping caudex and erect portion of stem
apex (Croat 60613). —B. Po ed n showing habit and leaves with variegated blades and inflorescences at anthesis
(6 roat 69695). ме; Clos e-up we crown of slant with abaxial surfaces of blades and side view of the spathe (Croat
3921). a puc nii liie f ree-ending, inequilateral sheath and acutely sulcate free portion above sheath

. —Е. «n of plant showing speckled petioles and in flore 'scence at anthesis (Croat 77298). —F. Spathe

E . cut open to grin inner surface of tube. —G. Close-up of inflorescence showing apical half with spathe
blade somewhat spre "Po and staminate рене of айк protruding somewhat forward. —H. Portion of spadix showing

bicarpellate pistils. F. С. Н. (Croat 7182€

748

Annals of the
Missouri Botanical Garden

ир ee Schott, Bonplandia 7:
Dieffenbachia seguine subvar. ventenatiana
: go ahrb. Syst. 20: 508. 1899. Dief-
"Pflanzenr. IV. 23 De(Heft 6 90 18. 1915. TYPE: Su—
riname. Without locality, Hostmann s.n. (holotype,
ej

м 'nbachia 50 Mart. ex Schott, Prod. Syst. Aroid.

60. Dieffenbachia кн var. ates

Ай. ex Schott) ingl., FI. Bras. 3(2): 175. 1878
Dieffenbachia жй re var. (Se hott)
A 570 Jahrb. 568. 1899. TYPE: Brazil.

Marti tius 2 шз a
bife irrorata Schott, Prod. Syst. b 335.
800. Die 5 seguine fo. irrorata (Schott)
т Fl. Bras. 3(2): 1185 €
> subvar. irrorata (Se
st. 26: 568. 1899. Pees seguine subvar.
ти ES hott) Engl., Pflanzenr. IV, 23 Dc(Heft 64):
3. TYPE: Brazil. Pará: C. Martius 2640 (ho-
nnd P
Dieffenbachia conspurcata Schott, J. Bot. 2: 52. 1864.
Dieffenbachia seguine fo. conspurcata (Schott) Engl.,
Fl. Bras. 3(2): 175. 1878. TYPE: Brazil. Рага: Schott
paintings i & B x0 агі the 65 ha & Ьб)
se designated her
Dieffe nae hia a uranium Verschaff. & Lem., Ti Hort.
l +F mbachia seguine fo. barra-
AP i chal . & Lem.) Engl., Fl. Bras. 3(2):
174. 1878 Dieffenbachia seguine subvar. эфа
тапа a (Versch Lem.) Engl., Bot. Jahrb. Syst.
2 1899, Dieffénbachis ые var. foram.
2:

type (lectotype,

w
=
=

л
Cc
FA

ana postera & Lem.) Engl., Pflanz IV,
De(Heft 64): 50. 1915. ue not designate the
illustration in III. Hort. 387. 1864, serves as

totype, designate ч һеге).
d iet a Verschaff. n Hort. 13: t. 470,
186€ 5 75 subvar. gigantea
ne rschaff. ) Engl., Bot. Jahrb. 26. 569. 18 di ТҮ РЕ:
not designated; the illustration i in III. Hort. 13: 470—
85 a 06, serves as the type (lectotype, 1 d

type (lec

hiuc wallisii Linden, III. Hort. 17: t. 11. 1870.
ffenbachia seguine subvar. wallisii (Linden)

Er i 2 lee enr. IV 23 De(Heft 64): 47. 1915.
TYPE: Brazil. Rio Negro, 1866, Wallis s.n. (holotype,

K!).

Dieffenbachia brasiliensis Veitch, Cat. 12. 1875. Vie al
асга picta fo. go dia (Veitch) Engl. . Bras.
3(2): 176. 1878. TYPE: Brazil. Not isa d;

of Veitch Cat. serves as the

х

e n p. i
(le e, designated here).
hieu picturata L. Linden & Rodigas, Ш. Hort.
: 101.1. 163. [CLXIII 1892. Dieffenbachia rie
a subvar. picturata Engl., Bot. Jahrb. Syst. 26:
570. 1899. uv Venezue D pie in III.
foil vol. 39: t. 163. 1 55 serves as the type (lec-
type, de СЕЕ here
Ditch seguine (Jacq. E^ ‘hott subvar. ecu
Schott) F ‚ Jahrb. Syst. 26: 568. ). Dief-
. к, уаг. 1 apaa
Pflanzenr. IV. 23 1 uk ft € |
1915. Dieffenbachia ventenatiana Schott, b.
dia 7: 30. . TYPE: Suriname. . (K)).

E.
ya

Herb, to 1.5

internodes 1.7-5 X

> m tall; stems reclining at base then

erect: .5—4.0 cm. medium

green and glossy soon becoming dark green, se-
miglossy to almost matte, smooth. LEAVES arching;
petioles 10—34.5 cm long, averaging 29.7 cm long.
medium green and weakly glossy, rarely white,
sometimes densely pale green maculate, sheathed
25—V. or more their length, free part of petiole 5—7
em long, acutely sulcate; sheath 20-28 long, pale
green and matte on inside, usually acute on one
side, rounded on the other side, sometimes inequi-
aterally acute on both sides, curved inward along
the margins but the sides not contacting, faintly
striate throughout but especially noticeable toward
the base, the basal portion of the sheath often per-
sisting after much of the petiole falls free: blades
ovate-lanceolate, 17—38.5 ст long. 10-20 ст wide
(averaging 32.1 X 17.3 cm), 2.7-3.3 times longer
than wide, 1.2-1.6 times longer than petioles, ine-
quilateral, one side 1.5 em broader, inequilaterally

rounded at base or with one side acute the other
rounded, subcoriaceous, semiglossy, medium-dark
green, sometimes mottled with pale green or white,
especially along midrib, moderately paler below:
midrib flattened-convex and slightly paler, ca. 6
mm wide above, narrowly rounded and slightly pal-
er below, sometimes darker green-maculate in low-
er half: primary lateral veins 13 to 15(19) per side,
arising at 4050? angle, quilted-sunken and con-
colorous above, concolorous and concave below; in-
terprimary veins usually present and nearly as con-
spicuous as primary lateral veins: minor veins
moderately indistinct, arising from the midrib and
paralleling the primary lateral veins. INFLORES-
CENCES 1 to 4 per axil, usually solid green but
sometimes pale greenish yellow maculate through-
out (maculations sometimes appearing in irregular
transverse rows on spathe); peduncles 2.5-14 cm
long, 7-8 X 8-12 mm diam., medium green, weak-
ly glossy, faintly dark green-striate; spathe 11-24
em long, abruptly acuminate at apex, gradually
constricted above tube, in the upper 25. medium-
dark green and semiglossy to matte outside, slightly
paler and glossy within; spathe blade at anthesis
stiffly erect then recurving near apex; spathe tube
7-10 ст long, 1.2-1.8 X 2.0-2.5 cm diam.; spadix
10-19 cm long; the naked portion at base 1.5-2.5
cm long: pistillate portion of spadix 4-8.5 em long:
pistils 20 to 25
10-12 mm, with up to 3 of them in a loose spiral

. closely aggregated except in upper

across the spadix but usually with | or 2 at any
level on the spadix; ovary bicarpellate, markedly
bilobate, rarely 3- or 4-locular (and 3- to 4-lobate,
respectively), pale green, semiglossy, 3.2-3.6

2.1-2.4 mm; stigmas pale orange, doubled (one for
each locule) but usually fused along the adjoining
margins, 2.3—4.3 X 2.0-2.4 mm diam.:

—

staminodia

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

4 per pistil, 2.8-3.1 mm long, 0.8-1.0 mm wide at
apex, slightly thickened toward apex, flattened and
free at base, the base equally as wide or up to twice
as wide as the apex; fertile staminate portion of
spadix 5-7.5 cm long, 5-15 mm diam., slightly
broader midway, tapering slightly toward both ends,
bluntly acute to rounded at apex, at anthesis pro-
truding forward out of spathe and usually being
trapped there by the closing spathe; staminate flow-
ers 5 to 6(8?) per spiral, (1.6)2.2-3.5(4) mm diam.,
squarely rounded to rounded, sometimes broadest
perpendicular to the axis, smoothly rounded at
apex. sometimes with a transverse linear slit me-
dially; anthers 5 to 6 per synandrium, shedding
their pollen well below the rim of the synandrium;
the mostly naked portion of spadix 2.0—4.0 cm long,
6—8 mm diam., medium green with 1 pistil in lower
%4 and with 2 to 3 staminodes in upper Y, some-
times with only a few staminodia scattered in upper
34. Berries bright red or orange.

Distribution and habitat. Dieffenbachia seguine
ranges throughout much of the West Indies from
Cuba (Ileana Arias, Havana, pers. comm.), Jamai-
ca, Hispaniola, and Puerto Rico, through the Lesser
Antilles to Trinidad and South America, there rang-
ing throughout much of Venezuela (Amazonas, Ar-
agua, Apure, Bolívar, Carabobo, Delta Amacuro,
Distrito Federal, Falcón, Lara, Miranda, Monagas.
Nueva Esparta, Portuguesa, Sucre, Táchira, Truji-
llo, Yaracuy. Zulia), especially in the Cordillera de
la Costa, to Guyana and Suriname (Boggen et al.,
1992), French Guiana, eastern Brazil (Amapá,
Amazonas, Goiás, Maranhão, Pará, Rondônia, Sao
Paulo), and west to the lowlands of Colombia (Meta,
Vaupes, Vichada), eastern Ecuador (Маро), and Bo-
livia (Pando, Santa Cruz).

Dieffenbachia seguine flowers and develops ma-
ture fruit to some extent all year-round, but with
more flowering occurring in the late dry season and
throughout the early part of the dry season between
March and September.

The species is characterized by having petioles
that are shorter than the blade and sharply sulcate
on the free portion, with the sheath margins acute
to rounded at the apex and with ovate-lanceolate
blades. The best character for separation of the spe-
cies, however, is the unusual inflorescence with
large, bicarpellate ovaries and a spathe that is
somewhat spread backward while the staminate
portion of the spadix protrudes prominently forward
and persists after the spathe has closed.

The species was long considered to be a common
species in Central America but that material proved
to be mostly D. oerstedii, and in some cases, D.

wendlandii. The latter species was even erroneous-
ly synonymized with D. seguine by Engler (1915).
Both species sometimes have blades of similar
shape, and both have petioles that are comparably
sheathed and sometimes sharply C-shaped on the
free portion. However, D. wendlandu differs in hav-
ing pistils with a single ovule. The staminate spadix
of D. wendlandii is also more or less tapered toward
the apex and not protruding strongly forward at an-
thesis, whereas in D. seguine the spadix is stubby-
ellipsoid.

| agree with Bunting (1979), who synonymized
both D. picta Schott and D. maculata (Lodd.) €.
Don under D. seguine. This species has been the
most confusing of all Araceae in the number of ep-
ithets (subspecies, varieties, subvarieties, and
forms) recognized, over 60 in all. Some are varieties
of D. picta, others varieties of D. seguine or com-
binations between the same two taxa. It is not clear
why this should be so. Throughout its range it is
no more variable than any other species of Dieffen-
bachia, but it is quite widespread and this brings
it into contact with more workers. Most of the ep-
ithets were based on Schott names, but Engler
treated most of these as varieties or subvarieties of
D. seguine or D. picta. All of the taxa involved
share a suite of characters that make it unique,
namely the sharply sulcate petioles, the protruding
and thickened staminate portion of the spadix, and
bicarpellate ovaries.

A cultivated collection from Grenada (Croat
77298) had sap that was celery-scented, not at all
smelling of oxalic acid, typical of so many Dieffen-
bachia species. Croat 78323, from Venezuela, also
has a sweet- rather than a foul-scented sap.

Engler (1915) placed Dieffenbachia lancifolia
Linden & André into synonymy with D. picta, but
the former is a distinct species from Antioquia De-
partment, Colombia. Also excluded are combina-
tions of the name, Dieffenbachia picta Schott forma
lancifolia (Linden & André) Engl. and D. picta
Schott subvar. lancifolia (Lind. & André) Engl.

Also erroneously placed in synonymy with D.
picta was Dieffenbachia meleagris Linden & Rodi-
gas and the combination subvariety meleagris Engl.
That species is from Ecuador (see illustration 159
in Ill. Hort.) and looks like it might be synonymous
with D. spruceana Schott.

Dieffenbachia shuttleworthiana Engl. was syn-
onymized with D. picta but should be excluded
along with the following combinations: D. picta for-
ma schuttleworthiana (Regel) Engl. and D. shuttle-
worthiana Hort. . This Colombian species is

not closely related to D. seguine.

750

Annals of the
Missouri Botanical Garden

Additional specimens examined. о 1202 (К). Ca-
det 6030 (К). BOLIVIA. Pando: Nicolas Suáre 2,
km N of Cobija, Beck 17103 (L a "MO.
Velasco, 10 km SE of buildings of Est. Flor de Oro
41364 (MO, NY). BRAZII K. P). Engler 227
(K. rae Mato Grosso Sul: Catharino et al. 1909 (SP).
ш Mpio. Capanema, Rio Quatipuru, near Mir

30 km by rd. of Braganga, Davidse et al. 18102
(MO): Río Anajás, Ta ie sta Alegre, Cuanta do Anajás,
Beck et al. 29 Y); Río Anajás, Ilha do Marajó, Prance
et al. 30247 1 0 een а Floresta do Oeste,
Rodovia P-50, Goncalves et al. 224 (MO). Sao Paulo: Sao
Paulo, Instituto де Botanica fa е Paulo, Secáo de Fi-
toecologia, Lotto s.n. (К, MO). COLOMBIA. Vaupes: Río
Kuduyari, bola of Río Vaupes, Schultes & Cabrera
17890 (NY). Vichada: Río Meta, Manati,
4225 (US). ECUADOR. Napo: Auca Oil Field, Ingram
1169 (MO, SEL). FRENCH GUIANA. Vic. of Saúl, route
to Béllizon, 100-300 m past Faux Claires, Croat 74137
S US, VEN); Piste de Bélizon, pk 21.8, Billiet et al.

7 (MO): Crique Gabaret, bassin de POyapock, Cremers
s (CAY, К). Cayenne: Colline de Montravel, Пе de
Cayenne, Le Goff A. 95 (CAY, MO); Piste de Saint-Elie,
15.7 km S of ORSTOM camp, Prevost 3258 (CAY, MO),
Prevost 3580 (CAY, MO); Centre ORSTOM de Cayenne,
Prévost 3382 (CAY, MO); Saint- Laurent-du-Maroni, Saül,
trail to Mont Galbao. Mori & Gracie 18717 (MO, NY).
. Loreto: Alto Amazonas, Dtto. Manseric HE
de Manseriche, R. Rojas et al. 607 (B, MO,
VENEZUELA. ее Río Guainia, 5 of s Ma-
guire et al. 36461 (NY); Cano Mosquito, Cano Marieta,
Lister & Colchester 272 (K); Tencua, Colchester 2108 (К);
Dpto. Atabapo, Río Cunuc unuma, Raudal Picure, J. Pérez
«€ M. Sosa 671 (MO); Cano Majagua, E. & S. Zent 2189
(MO); Casiquiare, Río Cuainis, Bunting et al. 4108 (NY);
i SE of Puerto Ayacu-

^
S
+

"
=
y
=
—
> E
Y

Cuatrecasas

۲ ongo

„ Río Arauca, 5 km SW
González 1341 ) (MO). Aragua: betw. \
mare de la Costa, Henry Pittier NP, a km N of summit,
Croat 60567 (СМ. F, MO); Pittier Park, Paraiso trail to
Pico Periquito, Croat 21412 (MO); Ocumare-Portachuelo,
Steyermark & Rogers 119364 (MO, USS); 5
Paraiso Trail, near Rancho Grande, Bunting et al. 1937A
A Y): Rancho Grande to the Toma, Bunting et al. o

; 12 km NW of Rancho oe Bunting 2035 (NY),
Mois 2036 (NY), Bunting 2622 ; Maracay, campos
de la Facultad de Agronomía у Centro IR Investigaciones
Agrícolas, Univ. Central de Venezuela, near Pozo del Dia-
blo, Hunting 2026A
NY

Sabana, El Dorado- pue Elena, km 202, 5 of Salto Ката,
Davidse et al. 4844 (MO); base of Altiplanicie de Nuria,
Bunting & Папин 4319 (NY); W of Hato de Nuria,
са ; 88864 ‚ US); Río Karuai, base of Sororo-
W of La KA Steye jori 60796 (NY); near El
5 Èm S of Caño Paso Ancho, Bunting & Trujillo
2236 (NY): Kamarata, Bogner 965 (M). Carabobo: PN
San Esteban, Río San Esteban. Benitez de Rojas et al.
4661 (MO, MY); Río San Gian, 5-6 km 5 of Borburata,
Steyermark 94331 (MO, US). Delta Amacuro: Río Ama-
curo between “vuelta larga” and Cerro Wuausa, Dept. An-
tonio, Trujillo ег al. 17397 (MY). Distrito Federal: Fila
Las Delicias above Naiguatá, Bunting & Manara 21241
(NY), Drake 7 (Р, US); Cerro Naiguatá, 6 km SW de los

tanques de la Electricidad de Caracas (Cocuizal), Steyer-

27170 (GH, MO, NY); El Aguacate,

mark 91896 (NY, US); Los Caracas-Higuerote Rd., be
tween km 5 and Osma, Bunting & Fernandez 329: 5 (NY):
Pico وو‎ Fila Las elici las Naiguatá, vic. Las Deli-

(NY), Bunting & Manara
„ (NY): Río San Julián, ist at Caraballeda, Bun-
ng 2044 (NY). Falcón: PN Quebrada de la Cueva El
Toro, Liesner et al. 7681 (MO). Ы Рио. Jiménez, PN
is ambü, Quebrada Negra, Davidse & González 21012
(MO). Miranda: Cerros del Bachiller, 5.5 km S of village
Santa Cruz on Hwy. 9 between Guatire e C rs Croat
53956 (М0); Cerros del Bachiller, near Е end, Т0 air km
W of Cúpira, Steyermark & Davidse 116647 (МО); PN
Guatopo, Fila la Guzmane ra, Santa Teresa-Altagracia de
A f rd. to Caucagua, Bunting el
al. 2072 ( agracia de Or-
ituco, Aristeguieta 1764 (NY), Croat 21741 (MO
cagua, 600 m, Bunting et al. 2073 (NY). Monagas: Mor-
ichal Las Tetas, tributary of Río Tonoro, near Aguasay,
Montes s.n. (MO); Caripe-Santa Ines Rd., ca. 3 km E of
Teresen, Colorado-Los Cigarrones, Río С 1 Bunting
2729 (NY); Juse E jn lona Hd., 6 km SW of Jusepin,
Bunting 2738 (М aripe- aes Rd., Bunting 2678

VY): Morichal E Y E Past Jusepín, M. Heredia 60 (MO).
Nueva Esparta: Margarita Island, Juan Griego trail, J
R. Johnston 305 (NY, US). Portuguesa: аруа Al-
garrobo, tributary of Río Morador, 7 km NE of Boca de
Monte, 22 km NE of Rio е Steyermark et al.
127204 (MO): Guanare-Biscucuy Rd., El P
above jet. of Guanare-Barinas rd.,
Рио. Araure, Río Auro (La Lucia), NW of Sta.
Aymard & ЖЕ 3090 (МО); Dtto. Guanare, Guanare-
Mesa de Cavacas, 1 et al. 7940 (MO,

( Я ‘| Pilar-Guariquén, El Pilar and Guari-
quén, 4-10 km 5 of k l Pilar, Croat 54380 MO). Táchira:
8 km S of El Pinal, Steyermark et al. 102036 (MO, MY);

San Cristóbal- hor del Indio, Caño Secto-La Florida,
kı m dn Sb San Cristóbal, Bunting 11687 (MO);
Las Min: of La Laguna, 16 km SE of Santa Ana,
1 & (iR 118891 (MO). Trujillo: Sabana-
Mendoza, ca. 5 km below Betijoque. 5 2829 (NY).
Yaracuy: Las Trincheras-El Cambur, N of Salom (NE of
Nirgua, W of Valencia) on rd. to Candelaria, Croat 54649
(CM, MO); Marín and Aroa, Sierra de Aroa, Dito. Felipe
between Albarico and Tesorero, 9.8 km N of jet. of hwy.
TU Sierra de Aroa, PN Yurubf,
| . Río Yurubf, Liesner & A. Gon-
zález 10126 (MO, NY): Si тта de Aroa, vic. Aracal, 7 km
above San Felipe, Bunting et al. 1997 (NY); ane La
Chapa, N of Nirgua, Steyermark & Bunting 97728 (NY);
Dtto. Nirgua-Dtto. San Felipe, Cerro La Chapa, 7 km N
of Nirgua, Davidse et al. 20914 au rro La T
Steyermark et al. 100213 (NY, US a Chapa, 5
ermark et al. 100318 (US), кл Ha 100239 (US)
Dito. Nirgua. Salom-La Candelaria Rd.,
lotal, Meier et al. 5164 (MO, VEN); Dtto. Bruzual,
Montafia de María Lionza, W of Sorte, Steyermark et al.
124955 (MO); Dtto. Sa Felipe, PN Yurubí, Aymard et al.
2714 (MO): Dtto. Urachiche, Quebrada Higueronal. W of
Urachiche, vic. Sabana de Méndez, Ss leo et. al.
124629 (MO); Río Guayabito, 15 km N of ín, Steyer-
mark & Bunting 105293 (MO). GREATER ANTILLES:
HAITI. Nash 611 (NY); massif de la Lelle, Port au Prince,
Mantflurry, Ekman 1983 (K). HISPAÑIOLA. SANTO DO-

NGO. San C аан Cordillera Central, San Crist6-

Cumbre Game-

ahona: Fuertes 564 (GH); Santo Domingo, Zanoni et al.
La Leonor, Moncion,

Volume 91, Number 4
2004

Croat 751

Revision of Dieffenbachia

Liogier 13307 (GH, NY); Carib Territory, Bataka, J. Hig-
gins 119 (MO, NY); Sierra de Baoruco, Arroyo La Travesia
near the La Travesia sugar mill, Zanoni et al. 25159 (MO,
NY). El Seibo: El Guaraguao-Los Hurados. Miches-Hig-
uey, km 15, Mejia & Romie: 9929 (MO, NY). Monsenor
Nouel Pobra Cordillera Central, Río Yuboa, Zanoni
et al. 113 (MO, NY): Cordillera Oriental, Arrovo de
Agua, me | km V of El Valle. Croat 68494 (MO): 9.2 km
SE of Miches, n Rio Ye ica Arroyo Santi ago, Croat
68547A (JBSD. K. MO). Samana: 2.3 km S of Playa El
Valle, Mejia & Zanoni 6614 MO, PNY): $ Sanchez, Las Can-
itas Mts., N. Taylor 48 (NY); Sanchez Ramirez, Rose et al.
4375 (NY); Rio Sis W of Cevicos, 22 km E of Cotui.
Zanoni & Pimentel 23420 (MO, NY). San Cristóbal: San
Cristóbal, a Jina (de Yamasa), 16 km del Parque Central
de Yamasa, Zanoni & 5 23456 (MO, NY): near
Rio Nigua, Lavastre 1845 (NY); near Nigua River, La
Toma, Augo 1693 (NY): Dajao. Bayaguana, Liogier &
ве г е (NY). JAMAICA. Port Anténio: Hitchcock
О); Fury River, Harris 8367 (NY); John Crow Mts..

ү 4126 (NY). Portland: bees i John Crow Mts..
W of Ecclesdown, Grayum et al. 9973 (K, MO). St. Eliz-
abeth: Frenchman, Proctor ders (NY). PUERTO RIC 2
Without exact locality: Engler 2793 (K), Sintenis P. 279:
(K). Britton & Britton 9664 (NY), Britton & Britton das

Y): Maricao, Sargent 643 (MO); San Sebastian. Sargent
340 (MO): Laguna Tortuguero, Howard & Nevling 16978
A); Quebrada dest El Verde Field Station in Luquillo
Experimenta For W side of Luquillo Mts., Whitehill 8
О); Luquillo de Мом Florida, km 28.1, R.
8 (A); Río ee State Forest, Hwy. 621.
(MO. NY, PMA, RSA); km 21.5 on Rte. 2, V
laria, Solomon e (MO); Mayaguez vic., Cowell 550
(NY). Britton & Shafer 1625 (NY). Britton & Britton
10082 (NY); Mpio. Maricao, Bo Indiera Fria. Rt. 125, 0.3
km S of Rt. pu Atha & Zanoni 770 (MO); Coamo, Wood-
bury et al. s.n. (MO); Caribbean Nat. For., ca. | km No
Río kor he Hwy. 186, Thompson 32 38 (MO): Mpio. Lu-
gillo. Route 988, 1 mi. E of intersection with rt. 983,
Miller & Taylor 5937 (MO); Río Piedras, Cowgill 532
(NY). LESSER ANTILLES: VIRGIN ISLANDS. St. John:
N Bordeaux Mountain, Coral Bay Closest 100 m from
communications tower,

=

Acevedo-Rodriguez 4705 (MO,
Y). Tortola: Carrot Bay, D'Arcy 769 (MO), Fishlock 326
(К). sT. KITTS. Britton 447 (NY). LEEWARD ISLANDS:
DOMINICA. Roseau-Sulfur Springs, Howard 11744 (A);
N of Calibishie, Hodge & Hodge 3174 (GH): Milton Es-
tate. Hodge 2929 (GH); Castle Bruce Valley, Beard 656
GH); St. Patrick iy Cote d'Or, Nicolson 2060 (GH).
Lloyd 237 (NY); St. Mark Parish, oa Springs area,
^ Hill лее Uu GRENADA. Horn, towards
Birch G , Simmonds s.n. (К). p ADELOUPE. Gua-
M ‘Duss 3790 (NY, US); Admdiv. Basse Terre, Piste
vers Je chute de Carbet, J. Billiet & B. dude 7359 rs
MO): Basse Terre, Grande Etang (Pres des s du Ca
bet), Billiet & pd 1357 (MO). Billiet : pes б, 7358
(BR, MO): Basse Terre, Crique Lézarde, Billiet & Jadin
7346 (BR, MO, Billie 9 Jadin 7347 (MO). Marie
ante: ravine of Riviere de St. edd Grand Bassin-Les
Balisiers, Proctor 20987 (A, US). WINDWARD Ж ANDS:
MARTIN IQUE. M. Hahn 945 (GH, K. P. US), P. Duss
21496 (NY). ST. LUCIA. Sturrock 352 (A): LÍ. Louvet
near nursery, Slane 634 (A), Howard 11564 (A). ST. VIN-
CENT. H. H. Smith & G. W. m = (К, NY). TRIN-
IDAD. cen Blanchisseuse rd., 4. Croat 53921
(HUA, K, MO, NY, TRIN, VEN):
Rd., near milepost 7 34, Philcox 8231 (К).

Gal-

pude Blanchisseuse

Cultivated specimens. Society Islands. Leeward. Ra-
RM in Uturoa, 17 Dec. 1926, J. W.
S.A. Hawaii: Honolulu, Kalihi Valley,

. 1956, de чу Neal s.n. (BISH); Foster Gardens,
1962, Miyashiro s.n. (BISH); Lyon pee ic 10
Sep: 1 1975, D. Herbst & S. Ishikawa 5459 (BISH): Oahu,
5 a 1954, Won s.n. (BISH); Honolulu. Kaimuki. | 5 May
Kapalama Heights, Kame ha-
, Judd et al. s.n. (BISH).
Missouri: Missouri Botanical Cardo n, originally obtained
from J. Henny, Apopka, Henny 7 (MO), Croat 78287 (MO):
13 Sep. 1990, Miller & Schmidt 5551 (MO). Puerto Rico.
Rio Abajo (originally чег by Thompson 3238), 19
. Hispañiola. Border of PN
os Haitises, 27 Apr. Do um n. (Holst 6237) (MO).
бл Originally collected by John Criswick, Grenville,
93. Croat 77298 (MO, VEN). Belize. Cayo:

17 *06'N. BOW, 24 Jan. 1990,

'enezuela. Carabobo: originally

iatea Island,

Grenada,
Nabatunic a near Sukkotz,
Balick et al. 2359 (MO).
collected by Bunting from a Garden in Valencia, 300—500
m. (Bunting 13515) Croat 78323 (MO, VEN): Jardín Bo-
tanico, Caracas, 19 Aug. 1976, Croat 38344 (MO).

24. Dieffenbachia standleyi Croat, sp. nov.
TYPE:

Нолан, d Botanical Gar-

hwy 15°44'N, ae 70-90 m. 9 Feb.
1987, T. B. Croat & D. Hannon 64638 (holo-
type. MO-3442883!; isotypes, BI. CAS!, COL!
EAP!, F!, GH!, INB!, K!, MEXU!, PMA!, NY!,

TEFH!, US!, USCG!). Figures 24, 28B.

Planta 0.6—1.5(3.0) m alta: D 3—6(10) em lon-
ga, 6-11 cm diam.; —52 cm longus; lamina
elliptica vel obovato- Mis a, dare em longa,
12.5-39 ст lata, nervis pou lateralibus 12-24. ut-
7 0 er axillam: a "ulus. ad

.5)15-29 cm longus; du 20—50 cm long

petiolus
inflorescentia 2—41

Terrestrial herb, frequently in streams or on
stream banks, 0.6—1.5(3.0) m tall; sap foul-smell-
ing. caustic and irritating; internodes 3-6(10) em
long. 6-11 cm diam., dark green, semiglossy: pet-
toles 12.5-52 cm long (averaging 26 cm long).

таце. light green, paler than stem, finely and
densely striate throughout, sheathing nearly always
to the base of the blade, the margin usually mark-
edly undulate and thin, sometimes with the apical
portion curled outward, otherwise erect, often dry-
ing undulate, free unsheathed portion 1-5 cm long
(averaging 2 cm long); blades elliptic to obovate-
elliptic, 31-84(103) em long, 12.5-39 cm wide (av-
eraging 54 X 23 cm), 1.7-3.1 times longer than
wide (averaging 2.5), 2.1—4.6 times longer than pet-
iole (averaging 3.2), inequilateral, one side 3—4 ст
wider, abruptly acuminate at apex, somewhat ine-
quilateral and acute to weakly attenuate or rounded
to obtuse at base, coriaceous, dark green and se-
miglossy to glossy above, paler green and matte be-
low, drying medium gray to dark brownish gray
above. paler and yellowish gray to pale yellow-

Annals of the
Missouri Botanical Garden

Figure 24. Dieffenbachia standleyi (Croat 42676). —A. Habit of cultivated plant. —B. Stem and base of leaves.
Ck

—C. Upper part of stem showing abaxial surface of leaf blade and cluster of inflorescences. —D. Close-up of petiole
bos 's showing the markedly undulate petiole sheaths.

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

brown below: midrib slightly paler and flat to sul-
cate and finely paler striped above (especially near
the base), sometimes white in distal 25, convex to
narrowly rounded, thicker than broad and paler to
slightly paler below, drying 8-12 mm wide, medium
yellow-brown, finely ribbed with the ribs minutely
and obscurely scabridulous on magnification: pri-
mary lateral veins 12 to 24 per side, arising at an
acute angle, then spreading at 40°-65°(70°) angle.
obtusely sunken and weakly quilted, paler toward
midrib above, bluntly angular and + concolorous
below, drying pale yellow-brown; lower surface with
minor veins moderately obscure, arising mostly
from the midrib but also from the primary lateral
veins. INFLORESCENCES 2 to 4 per axil: peduncle
to (7.5)15-29 cm long (averaging 16 cm long).
somewhat flattened; spathe matte, 20-50 ст long
averaging 28.3 cm long), 1.2-3.1 times longer than
the peduncle (averaging 1.6 times longer), 2.5

—
—
—

5—
em diam. spadix 20-30 em long (averaging 25
long): pistillate portion of spadix 12—13 em long:

cm

staminate portion 15-16 cm long. Fruits to | em
long. closely packed, reddish orange to scarlet at

maturity with the spathe light yellow.

Distribution and habitat. Dieffenbachia stan-
dleyi ranges from Honduras (Atlántida, Comayagua.
Cortes, El Paraíso, Gracias a Dios, Olancho, Yoro)
to Nicaragua (Matagalpa and Zelaya) at 30-1000
m elevation. Most collections in Honduras were
made in the Lancetilla Valley.

Phenology. Flowering specimens of D. standle-
yi have been seen from May through September,
although a few flowering collections were also made
as early as February and March. Fruits start to de-
velop in February and reach full size during March
or April (in Nicaraguan collections) or July-August
(in Honduras).

Discussion.
stout stem, fully winged petioles, yellow-brown-dry-
ing ovate-elliptic blades with 12 to 24 pairs of pri-
mary lateral veins, and a long spathe (20—50 cm).
It is most easily confused with D. horichii and may

The species is characterized by its

ultimately prove to be inseparable from that spe-
cies. Dieffenbachia horichii differs in having shorter
petioles with the sheath involute and moderately
smooth, in contrast to the petiole sheaths erect and
even curled outward as well as being undulate
along the margins in D. standleyi.

A collection by Stevens et al. 20998 from Mata-
galpa is unusual in being described as 3 m tall with
a trunk 10 em in diameter. Another Stevens col-
lection (7457) from Zelaya Department is notewor-
thy in drying darker yellow-brown than other col-

lections.

Specimens from Nicaragua differ somewhat from
those in Honduras, having leaf blades smaller on
average, ranging from 37 to 69 cm long and 13 to
31 cm wide (averaging 51 X 22.3 cm), but the
The

Honduran populations have petioles consistently

petioles in both areas average 30 cm long.

fully sheathed, whereas plants in Nicaragua often
have a free portion of the petiole above the sheath
ranging from | to 9 cm (averaging 4.4 em long) with
the petioles only rarely fully sheathed.

Blade shape is quite. variable. Blades can be
from 1.9 to 2.8 times longer than wide on the same
plant (e.g., Croat & Hannon 64638). Plants from
the Lancetilla Valley in Honduras have proportion-
ately longer blades, with some plants having blades
up to 3.2 times longer than wide (Croat 42676
Specimens collected at Lancetilla and its ийт
ings have blades that range from 1.9 to 3.5 times
longer than wide (averaging 2.5 times longer than
wide). Specimens from areas other than Lancetilla.
and outside Honduras, have blades 1.6 to 2.7 times
longer than wide (averaging 2.1 times longer than
wide).

A collection from Zulia, Venezuela, between La
Fría and San Juan de Colón (Croat 78289) differs
in having the petiole less fully sheathed and in hav-
ing narrower blades up to 2.6 times longer than
broad and drying somewhat less blackened. It may
prove to be the same species. If so, it would be the
only Central American species (with the possible
exception of D. killipii) that ranges from Central
America to Venezuela.

Etymology. Dieffenbachia standleyi was first
collected in 1928 by Paul Standley at Lancetilla.
Honduras. Standley was not only the author of most
of the aroid treatments for most existing Central
American floras, but he also described a number
of new species of Araceae, as well as collecting
several paratypes of D. standleyi. The species is

named in his honor.

Paratypes. HONDURAS. Atlántida: 5 km S of La
Ce pie е 705 (GH); near Lancetilla, Yuncker 4961
(F, ‚ NY); Lancetilla valley, ie Tela, ae 2124
sr. near Puente Alto ap on S. F. R. R. f Ceiba,
Yuncker et al. 8551 (F, ‚ MO, Y. US):
Tela, Webster et al. n 1 Tela, near Rio Lan-
сепа, above Exp. St., EU et t al. 3303 (MO, NY,
I): Tela, ca. 10 mi. SE of Tela along Río Lancetilla,
Єгові 42625 (MO). Croat 42676 (MO), Standley 53146 (F,
US). a: Siguatepeque, Standley & Chacon
6701 (F). Cortes: 2-3 mi. SW of Omoa on rd. from Puerto
Cortes to Guatemalan border, Croat 42556 (MO); El Par-
aíso, Yuscarán, Río de los Aguacates, Standley 25700
(КАР). Gracias a Dios: Ahuas Bila, 200 km SW of
Р uerto Lempira, Nelson & Cruz 9291 (TEFH, UNAH, US).
Olancho: Catacamas, Standley 18786 (EAP); ыр т
Olancho, W of main Терис igalpa- Catacamas Hwy.,

—

Annals of the
Missouri Botanical Garden

km щи am т апа ond of Si nte Boquerón, 8.6 mi.
SW of Ca ‚ 6 mi. SW of Sta. Marfa del Real, Croat
& D. Han 64109 (INB. ME XU, MO, TEFH, US); along
Gualac 'o-San Esteban at Río San
alaco, » 8.7 7 mi. SW of San Es-
8); Río Olan-

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San Esteban-Bonito Oriental,
& E ares deis М

Grande: on a tributary of the Río Agua (Río
Wind : gd 4073 (MO). NICA A.
P Tom: и Neill 1571 (МО); ridge 0
11786 (CAS, MO. TEX): Маны zos de Pe nas Blane us "AE
side, drainage of Quebrada El Quebradon, Hda. San Mar-
tín, border with Departmento de Jinotega, Stevens et al.
20998 (MO); Matagalpa-Siuna, 1.5 km al NE de Los An-
geles, Moreno 17142 (MO): El Trébol, 7 km S of Peñas
Blancas, rd. to El Tuma, Moreno p Rollen p^ (MO).
Zelaya: Finca Waylawas, Pipoly 4476 S); Siuna-
Matagalpa, ca. km be v Es г lí jn Wand, са.
8.9 m be yond Rosa Grande La Balsama,

T

>

vens рат (Mi ): Tes: „С егг

ca, vie. Cacerio de Vitinia, Rueda & Do inodo 655 57 "(MO

25. Dieffenbachia 5
Novon 9: 497. 1909. ТҮРК:
Toro: Valle del "e cio, along Río Changuinola,

Croat & Grayum,

—

Panama: Bocas de
ca. 1 km above mouth of Río Teribe, vic. Teribe
Indian population, disturbed forest among co-
coa plantations, 9°21'40"N, 82731'40"W, less
than 100 m. 25 June 1994, J. B. Croat & С.
Zhu 76452 (holotype, MO-04611212!; isotypes,
AAU!, B!, BM!, BR!, CAS!, CM!, COL!, CR!,
DUKE!, F!, GH!, HUA!, INB!, ITIC!, JAUM!,
K!, L', LE, M!, MEXU!, NY!, P!, PMA!,
R!, RSA!, S!, SCZ!, SEL!,
TEX!, UB! US!, VEN!, WU). Figures 25.
29B.

usually to less

than 1 m tall; internodes 1.5—4.5(—6) em long, 1.5—
3(—4.5) em diam..

Terrestrial herb, 0.5—1.5 m tall,

usually solid dark to medium
green, sometimes faintly marbled with gray-green
;

=

r yellowish gray throughout (on plants that also
have streaked petioles), initially weakly glossy, be-
coming semiglossy to glossy, often with a subvelvety
sheen; petiole scars manila to white, curved down-
ward on the opposite side of the stem and ending
unevenly; petioles 10-24 cm long (averaging 17.6
cm long), held +
sometimes white to pale green at base). almost

erect, medium green (except
matte to weakly glossy, weakly striate (especially
near the base), narrowly rounded to obtusely an-
gular on abaxial surface and often white medially,
sometimes streaked in a

variegated pattern

throughout (this white coloration continuing onto
the midrib), sheathed virtually throughout; sheath
erect to involute (rolled inward throughout in age).
free-ending and unequally rounded at apex, pro-
longed to 2 cm beyond the base of blade; un-
sheathed part obsolete or rarely to 1 ст long (when
evident obtusely flattened); blades ovate to ovate-
(15-)25-48(-63)
em long, (8-)15-32 cm wide (averaging 34 X 16

elliptic or oblanceolate-elliptic,
cm), broadest near the middle, sometimes below,
1-2.5(-3.5) times
longer than wide (averaging 2.1 times longer than
wide), 1.9—3 times
to erect-spreading, inequilateral, one side 1-3 cm

frequently above the middle,
longer than petioles, spreading

wider than the other, gradually to abruptly acumi-
nate, sometimes acute at apex, inequilaterally cor-
dulate at base, one side sometimes broadly rounded
to obtuse, the other side cordulate, sometimes in-
equilaterally acute, subcoriaceous, often conspicu-
ously quilted, moderately bicolorous; upper surface
usually solid dark to medium green, sometimes
conspicuously to sparsely variegated with pale
green or pale yellow throughout much of the sur-
face, the mottling large or small, but somewhat re-
stricted to the area midway between the midrib and
margin, matte to weakly glossy, sometimes appear-
ing weakly velvety, drying gray-green to olive-green
or dark brown: lower surface much paler and matte
to weakly glossy, silvery-green, drying yellowish
green to yellow-brown below; midrib flat to broadly
rounded and moderately to strongly paler, pale
green or sometimes creamy white above (sometimes
only toward the apex), bluntly acute to obtusely an-
gular and paler, sometimes white or creamy white
below, (0.6—)1—1.7 em wide: primary lateral veins
(14 to)18 to 25(to 30) per side, arising at an acute
angle and spreading at 457—90*, sometimes reflexed
toward the base, prominently to weakly and ob-
tusely sunken above, convex to weakly raised and
darker than surface or concolorous below, some of
the lowermost with a weak fold near the base (Croat
& Grayum 60112), sometimes convex-pleated be-
low; interprimary veins almost as conspicuous as
the primaries; minor veins moderately to distinctly
visible, darker than surface below. INFLORES-
CENCES 1 to 2(to 4) per axil, often with two ori-
ented in opposite directions; peduncle (3-)6-17 cm
long (averaging 10.3 cm long), 7-8 mm diam.,
weakly glossy, dark to medium green, sometimes
with pale yellow-green streaks; spathe (12-)15-28
em long (averaging 20 cm long), 2-4 times as long
as peduncle, acuminate at apex, convolute to about
the middle in lower part, matte to weakly glossy
outside, glossy within, solid medium green on both
surfaces, gradually and weakly constricted some-

Volume 91, Number 4 Croat
2004 Revision of Dieffenbachia

X
25 mm
D o x ura

Figure 25. Dieffenbachia tonduzii. —A. Close-up of stem, showing both creeping p erect portions. —B. Habit
with inflorescences and variegated blades. —C. Crown of plant with open inflorescence. —D. Close-up of stem 1
petioles streaked with creamy white 3 lose-up of stem showing solid green pe oles — Е. “los se-up of spathe «i
the blade portion open (Croat & Zhu 76452, type plant). —G. Inflorescence open to show upper male flowers and
lower E of spadix with pistils and n (Croat 66533). A, В, C. (Croat & Zhu 76452, type plant); D, E.
(Croat 76450

756

Annals of the
Missouri Botanical Garden

what above the middle; spathe tube 1.5-3 cm diam.
when closed, 6.8-9 cm wide when flattened; con-
stricted area 4.3—4.5 cm wide flattened; spadix (9—
)16.5-25.5 em long, about as long as or up to 3.0
cm shorter than the spathe; free portion 7.8-8.5 cm
long; pistillate portion (4.8—)6—1 1.5
sterile portion sparsely flowered to naked (rarely
lacking, as in Croat 70768), 1.8—4.0(—8.5) em long
with 0.6—1.5 ст totally bare, the uppermost portion

5 em long; mostly

with a few staminodia, sometimes with a few scat-
tered staminodia throughout, the lower half some-
times with an occasional pistil and much reduced
staminodia, rarely with the female flowers + equi-
distant and nearly contiguous with staminate part
(Croat 70768); fertile staminate portion (4-)5.5—10
em long, 7-10 mm diam., slightly broader midway,
weakly tapering to apex and base, bluntly ee
at apex; staminate flowers 5 to 6 per spiral,

rounded in outline, crenulate along margins, trun-
cale al apex;
shaped, 1.8-2.5 mm diam. pistillate portion of spa-
dix to 11 em long, 9-10 mm diam.;

sterile male flowers irregularly

female flowers
(15 10)48 to 62, closely aggregated except in the
upper 1.5 cm of spadix, 4 to 5 across the width of
the spadix (uppermost pistil borne on an almost
bare segment of the spadix); pistils pale cream-yel-
3-3.5 mm
diam.; style (after stigma has fallen) sharply cupu-
liform,

low to pale yellow-green, smooth, 2.
1.5-1.7 mm diam. with a single central
pore; stigmas yellow; staminodia clavate, white, 2—
З mm long, mostly contiguous and sometimes fused
INFRUCTESCENCES with spathe pale

yellow; berries red to red-orange, 5-8 mm diam.

at base.

Distribution and habitat. Dieffenbachia tondu-
zii ranges from southeast. Nicaragua throughout
Central America to the Pacific slope of Colombia
(Antioquia, Chocó, Cauca, Valle) and Ecuador (Es-
meraldas, Loja, and Los Ríos), from sea level to
1400 m, in Tropical wet forest (T-wf) and Premon-
tane rain forest (P-rf) in Central America and
Tropical wet forest (T-wf) and Premontane wet forest
(P-wf) and Tropical wet forest transition to Premon-
tane (T-wf/P) in Colombia.

Phenology. tonduzii occurs
throughout most of the year with flowering collec-
tions seen from February through November. Most
collections have been made from April through Au-
gust.

Flowering in D.

According to the collections, fruits mature
throughout the year but with the greatest concen-
tration from October to January.

The species is characterized by its fully sheathed
petioles, usually matte to weakly glossy, sometimes
weakly velvety blades with cordulate bases and nu-

merous, broadly spreading primary lateral veins.

Because of the fully sheathed petioles it can be
confused only with D. horichii and D. crebripistil-
lata. Both of the latter typically have much larger
leaves that are not at all cordulate at the base
(though they are rarely broadly and weakly subcor-
date). Dieffenbachia tonduzii is polymorphic with
. oer-
stedii, and is quite variable in all respects. It ap-
pears, in Panama, to hybridize with D. oerstedii.
Croat & Zhu 76857C from the vicinity of Santa Fé
in Veraguas Province is apparently a hybrid. with
characteristics

regard to leaf markings in the same way as

intermediate between D. tonduzii
and D. oerstedii.

The species is similar to D. daguensis, a Col-
ombian species described from less than 200 m
elevation on the Río Dagua in Valle Department.
That species also has many rather close primary
lateral veins and a fully sheathed petiole but differs
in having the staminate and pistillate sections of
the spadix contiguous or nearly so. In addition, it
differs in having much shorter petioles (described
as being up to 5 cm long).

A South American species, D. parlatorei Linden
& André, also sometimes has petioles fully
sheathed, but differs from D. tonduzii in having leaf
blades usually broadest above the middle, semi-
glossy on the lower surface, and the midrib often
broadly rounded and spongy. It also has the primary
lateral veins arising at a 40°—60° angle from the
midrib (often at more than 60° and sometimes up
to 90° in D. tonduzii).

Croat 70900, from 250 m in Chocó Department
of Colombia, appears to be D. tonduzii but differs
in several ways. It has leaves with the midrib flat-
raised above with the margins undercut. It also has
stems that appear scurfy (though weakly glossy if
rubbed clean). Another difference is that the petiole
sheath is more prominently free-ending and sub-
acute at the apex. In addition, the free portion of
the petiole is broadly and sharply sulcate.

Additional specimens examir COSTA RICA. Alajue-
la: rd. to Coloma Virgen de | Socorro, Río Sarapiquí, Stevens
13564 (MO), Croat 68336 (CR, MEXU, MO, TEFH); Can-
tón de d Grayum & Murakami 9939 (CR, MO); Fin-

ca Los Ensayos 1 mi. NW of Zarcero, Croat 43629
(CM, MO); ( Cañas- pala, 10 km N of Bijagua, Croat 36472
(MO): Río Zapote, Cafias-Upala, Río Zapote, 4 km NNE of
Bijagua, Croat 36260 (MO); Cordillera de Tilarán, San Ra-
món-Bajo Rodríguez, Río Cataratitas, Croat 68097 (INB,
10); Cordillera de Tilarán, San Ramón-Bajo Rodríguez,
vic. of km 19.5 NW of San Ramón, Croat 78838 (MO); 17—
20 km NNW of San Ramón by rd. on way to San Lorenzo,
1-7 km N of Balsa, Liesner & ен 14797 (СК, МО);
San Ramón-Bajo e 36-37 km NW of San Ramón,
Croat 68196 (CM, MO, * m n along

wy. 15, 8 km NE of Сес Croat 46945 (К. MO, PMA);
Arenal Volcano, Funk et al. 10626 (C 4 p m et al.

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

757

10718 (CR); San rer Fortuna, ca. km 25, D. Smith et
al. 1059 (DUKE, MO); С и ra de Guanacaste, Montev-
erde, San ا‎ M Biol. a 1.5 km NE of Station, D.
Pues 633 (CR, INB, Tos Cordillera de Tilarán, Bosque
Eterno De Los Niños, Río Peñas Blancas, Laguna Poco Sol,
Haber & Zuchowski 11175 (CR, MO). Cartago: Tucur-
rique, Tonduz 12874 (G, US 5); Rio Naranjo, Finca El Cedral,
Vuelta, Tueurrique,
IS); 1.5 mi. E , 10.2 mi. NE of jet.
at Paraíso, p 47088 (MO); dong С amino Raiz de Hule,
SE of 5 0 Croat 36727 roat 50747 (MO),
у О); Cantón de Tri Rio Reve е
9469 (CR. MO Y): 3
“Los Espaveles” nature trail, Rio E
tazón, Liesner et al. 15330 (MO); Turrialba. Instituto зии
am., Lent 639 n Lent 694 (F); 12 km S of Turrialba by
| Pejibaye along Rio Gato, Liesner 14394
(MO): Tres Equis, 1.5 km E of Turrialba-Limón Hwy., Lies-
ner et al. i n PN Tapantí, Oropendola He: Nilsson
et al. 632 (CR); Oropendola trail, Nilsson et al. .
Monumento Nac ‘ional Gua R): Tos nto
‘Teresita, Rivera 1718 (CR, K).
‚ Standley & Valerio 45262 (US):
Stace & Valerio 45206 (US); Cordillera de
Gut aste, Rincón de la Vieja, near refugee Wer along
rd. A Quebrada Grande, Barringer et al. 4039 (F).
2 x E of San Ramón, ҮР 106 (м0) des Viejo-
Río Sucio, Croat 3575: ), PMA): La Selva, Puerto
Viejo de Sarapiquí, Croat 4431 : (MO); La Selva, OTS Field
Station on the Río Puerto Viejo just E of its jet. with th
Río Sarapiquí, тее 8874 (DUKE. F, MO), Grayum
2780 (DUKE, F. MO); La Selva, 6 km by rd. from Río Peje
crossing, : km SSE of Маѕаѕау, Schatz & Grayum 706
DUK rto Viejo just E of jet. with Río Sarapiquí.
Folsom hee (DUKE); Occidental trail, Kress 84-1630
1); Río Sucio, near Porto Viejo, Croat 35682 (MO); Zona
n N slopes of Volcán Barba, betw. Hío Peje and
Rio Guacimo, Grayum & Schatz 3174 (DUKE). Limón:
along hwy. from Turrialba to Limón, ca. Il mi. S of
Sic оа Croat 43333 (ISC, MO, РМА, WISC); Guapiles,
Leon 720 (F); Guapiles, Toro Aurarillo, p 20573 (CR):
Finca Anai, at headwaters of Quebrada Mata de Limón, W
of Mata de Limón (Sixaola region), Grayum & Schatz E 79
(CR, MO); Finca d Dodge & Goerger 9489 (M
km SW of BriBri, ;ómez el x 20405 (B. МО); dime
of Río 5 eh Río Reventazón, Shank & Мой
4288 (DUKE) mi. S of Punta Cahuita, ca. 3 mi. S of
turnoff to BriBri, А, 43201 (MO); Ref. Barra del Colo-
Hío Chirripócito- Río Sardina, Grayum 9504 (CR,

—
C
—
2х

yabo, Pérez 1 (€

—

3

rado,

. Robles 1158 (CR.
О); PN Tortuguero, Lomas de беш, 4 km NE of station
along Río Sierpe, Robles et al. 2050 (CR, G, MO): Tortu-
guero Cantón, BriBri-Suretka, Barringer 3525 (CR, F); Res
Indígena Talamanca, Sukut, mouth of Río Sukut at Rio
ren. Hammel et al. 17548 (CR, MO); Río Reventazón,
Finca Montecristo below Cairo, Standley & Valerio 48997
(US): Rio Segundo, Asunción, L. Gómez & Herrera 23477
(MO); Río хаба, BriB Bri-Caribbean coast, Baker & Burger
90 (Е, MO); Limón-Shiroles, Río Sixaola, 0.9 mi. SW of
Bambu, 6.5 mi. SW of BriBri, Croat 43298 (MO): Río Six-
aola, ca. 0.5 mi. SW of Bambu, ca. 3 mi. NE of Bratsi,
Croat 43266 (CR, MO); I 5 pes BriBri-Sixaola,
„); Cordillera
de Talamanca, headwaters of бы ifa Kake beta below di-
vide between Río Xikiari and Río Boyei, Grayum 10858

—

W of Paraiso, Barringer et dl. 3479 (CR

—

CR, INB, pr Puntarenas: Cordillera de ran Bosque
Eterno De Niños, Laguna Poco Sol, 18 km ENE of
Monteverde, -— et al. 10824 (CR, INB). Es José: Cañ-
ón del Río Grande de Orosi, Chacón et al. 1488 (CR, MO);
La Hondura, Standley 36314 (US); Vázquez de Coronado,
Braulio Carrillo NP, along Hwy. San José to Siquirres, along
trail to Río Sucio, site of the Old Carillo Ta Croat
78787 (MO). NICARAGUA. Río San Juan: “Los Filos”
near р Los Filos, Rfo Santa Cruz, Salick 8153 (MO).
Zelaya: 6.3 km S of bridge at Colonia Yolaina and ca.
0.8 km 5 of ridge of Serranías de Yolaina on rd. to Colonia
Manantiales, Colonia Somoza, ede Ang Río Pun-
ta Gorda, Atlanta, mouth of Caño el Guineo, Moreno &
Sandino 12855 (MO), Moreno & Sandino 12891 (МО); Río
Punta Gorda, Atlanta, Caño Negro mouth of Río r
Moreno & Sandino 12917 (MO); Rfo Punta Gorda, Atlar
mouth of rs fio del Oro at Río Chiquito, Moreno & Sanding
12955 (MO): Rfo W Gorda, Caño El Guineo, Tellez et
al. 4875 (MEXU, :
trail, Parque Intl. ү Аийда, from Quebrada Boca Chica
to Quebrada Bonyic, Polanco 1615 (PMA); 7.7 mi. W of
Chiriquí Grande, 1.5 mi. W of Punta Pena, Croat & Grayum
60112 (CR, MEXU, MO, PMA); Chiriquí Grande-Fortuna,
13.2 mi. W of Chiriquí Grande, Croat Т Grayum 60139 (B,
MO, PMA); Fortuna- eis Grande Hwy. near Cont. Div.,
Croat pe 00% 60355 (MO):
Chiriquf Grande-Fortuna, above rfall, 1.6 mi. N of
Cont. Div., Croat & Zhu 76450 (CR. MO. PMA, SCZ, US);
Changuinola, near Luzon, Kennedy 3253 (MO); Changuin-
ola- Almir: inte, Mile 7.5, Croat & Porter 16249 (MO); Gual-
aca-Chiriquí Grande, 6.6 mi. N of bridge over Fortuna
Lake, Croat 66732 (MO); Gualaca-C наг Grande, 1.6 mi.
N of Cont. Div, Croat. 74930 (MO); Gualaca-Chiriquí
8.1 mi. > of Punta Pefia, Croat 74952 (MO); N of
Fortuna Dam, McPherson 11129 (MO); rd. to Chiriquí
rande. TT 7371 (MO); 5.3 mi. N of Fortuna Dam,
then 1.4 mi. W along gravel rd. to Cont. Div. trail, Croat &
Zhu 76328 (MO, PMA); along Cont. Div. trail, McPherson
9865 (MO); Fortuna Dam-Chiriquí Grande, 1 mi. from Cont.
Div.. priar & Churchill 6252 (MO); Río А rie rar Кїп-
ca St. Louis-Konkintoé, Woodson Jr. et al. 9 (F, MO).
buie Gualaca-Fortuna Dam, 10 mi. Ne ji Los Planes 8
de Hornito, Croat 50049 (CR, MO); vic.
Rio С м, 67 70 66533 (B. CM, ENC
. MO. NY, OOMOTO, QCA, SAR, TEX, US); 4.5-5 е
N of Fortuna Fins Croat & Grayum 60070 (INB, МО); 7
mi. bevond (NW of) Los Planes de Hornito, Croat 4115
O): Gualaca-Bocas del Toro border, km 11
iN А); F ortuna Dam site N of f Gualaca, 7.7 mi. bed Los

.] mi. from main

Grande,

~

"s Antes, La 1 inca

~~
=a ав
[т]
«ч
—

JB). Darién: Mamey, Whitefoord & Eddy 372

(BM, MO, PMA). San Blas: Rio E nila, 10 km WSW of
Puerto Obaldía, Mori et al. 6814 (MO). Veraguas: valley
of Río Dos Bocas, 11 km from Escuela Agrícola Alto Piedra
(above Santa Fe) on rd. to C чой уш Croat 27490 (МО);
NW of Santa Fe, 11 km fi tela Agrícola Alto de
Mori et al. 3817 (

MO): 0.6 mi. beyond Escuela Nena «n Alto Piedra, Croat
& Folsom 53989 (MO); 1.7 mi. past Alto Piedra School,
Croat & Zhu 76858 (MO, PMA); beyond Escuela Agrícola
Alto Piedra, Croat 49070 (MO); 3-5 mi. N of Santa Fe,

Gentry 3035 (MO); vic. Escuela Agricultura Alto Piedra

near, Antonio 2994 (MO); 0.6 mi Батона Escuela Agrícola
Alto Piedra, Croat & Folsom 34042 (MO); Cerro Tute re-

serve, along ridge to summit, Croat 66993 (HUA, MO,

758 Annals of the

Missouri Botanical Garden
PMA); trail to top of Cerro Tute, Croat 48903 (MO, PMA); de Bimbe, Croat 57000 (CM, MO); Centinela, 12 km E of
Cerro Tute, Sytsma & Antonio 3006 (MO). COLOMBIA. atricia Pilar on border with те Ríos, Gentry 26705 (МО);
Antioquia: Murrf, La Blanquita, Río Murrí, Transect 7, Centinela, Montañas de lla, 1 E of Patricia Pilar, ca.

Gentry et al. 75903 (MO);
Barkley 17115 (COL); PN Natural “
ados arriba, Río Venados, A. ( a el d 3462 (JAUM,
MO); Mutatá, Río Chontadural, Hac ienda El Darién, Fon-
negra 1344 (HUA); Carepa, Est. Exp. de Tulenapa (CA),
Callejas et al. 9704 (NY). Chocó: Se rranía de Baudo, Las
Animas-Pato, Río Pato, ca. 4 km SW of Pato, Croat 56112
(CHOCO, JAUM, K, MO); Medellín- Quibdó, km 208.5, 9
km W of 190 ft з 9 km E of Quibdó, Croat 56205
(CHOCO, COL, ‚ HUA, MO); Quibdó- s. in, km
185, 14 km E » ns ndo, Croat 56282 (CHOCO, COL,
JAUM, MO, PMA); San José del A E Santa
Rosa, Croat 56625 (COL, HUA, MO); Quibdó- Mede Пп, 25
mi. E of Quibdó, Croat 52300 (F, MO, PMA); ca. 2 km E
of Playa de Oro, Croat 57427 (CHOCO, MO); Pub Rico
5 is (Chocó), Quebrada Antón, 15 km W of
Santa Cecilia W of Chocó-Risaralda ee r, Croat
70900 (MO); ш llín-Quibdó, 85 km W hes Bolivar, Croat
49310 (МО); Aci andí-Serrat via del Darién, Juncosa 619
(MO); Pueblo Rico (Risaralda)-Istmina (С 1900
Guarato and Río Guarato at Risaralda and Chocó border,
1 70868 (CM, MO); iss Quebrada € nig Galeano
4600 (MO); Arusí, El Amargal, trail to Arus ora 51
(COL), Croat & Mora 83696 (MO); Quibdó, pie dos Alto
del Viente Rd., 25 km N of Quibdó, Callejas & Jangoux
2692 (HUA). Nariño: Río Timbiquí. iie 8876 (K);
valle y of Río Imbi, Pasto-Tumaco, vic. “Palm 3 km NW
n E of Texas ( е Ріре Jine Manie nance
Cee 71461 (MO). Risaralda: Pueblo
Quebrada La Calera, Betancur et al.
3054 (MO). Valle. del Cauca: Cali-Bue aventura,
guerrero-Cisneros, Que кыт Guinea at 1.2
neros, Croat 62831 (COL, HUA, MO. UB); vic.
Rfo Cava, Croat & Gaskin 1 1 (CUVC, MO); Cordillera
Occidental, Río Digua, Cuatrecasas 15053 (US); Bajo nos
ima, Buenaventura-Malaga, km 51.3, Croat. 71017 (
Buenaventura- а Pulpapel fac Pu at km 9, ud
70099 E ECUADOR. Esmeraldas: San Lorenzo, Rio
Palavi, AWA encampment, Hoover el 12 3161 (MO);
Awá camp to pr jon Hoover et al. 3968 (MO); Lita-San
1 W of Río Lita Bridge (below Lita),
; 17. 3 km E of Río Tululbí, Croat
83126 (MO, ey 3: . San Loren
n е José, km N Lita-San Lorenzo rd, p 8. 3889
(AAU, К, GB, v NY, QCA, 5): Lita-San Lorenzo Rd., 1.2
i М. of El Durango, 21.1 km W of Alto Tambo, 2 el
al. 82441 (MO, ОСМЕ); Lita-Carondelet Rd., km 16,
Schwerdtfeger 21422 (MO); Bilsa Biol. Res., Montañas de
Mache, 35 km W of о 5 km № of Santa Isabela,
Pitman & Bass 995 (M NE); Fila de Bilsa, 7 km E
of San José de Bilsa, ca. 1 jn due SW of Esmeraldas, 12
km SE of El Salto on Atacames-Muisne Rd., Gentry et al.
72955 (MO); Eloy Alfaro, comuna de Corriente Grande (Río
C "Sd tributary del Cayapas), Yanez et al. 1387 (MO)
. Cotacachi-Cayapas, Charco Vicente, Río San Mi-
guel, Palucios & Tirado 11287 (MO, QCNE); Quininde,
Herrera-Los Monos, he pim TS of Río Aguacatal, Palacios
13626 (CM, MO, QCNE, US); NE of Las ( ei Sitio
La Bella Jungla, C гоор erativa Unidos Vencere
11452 (MO, QCNE). Loja: Río Pichimá, us 719 (COL,
MO). Pichincha: Río Palenque Science Center, halfway
between Quevedo and Santo Dominga de los Colorados,
Gentry et al. 24700 (MC
rd. (beginning 10.5 km N of Patricia Pilar), Caserío Palmar

T

Lorenzo rd.,

=

—

)); rd. E of Santo Domingo-Quevedo

| km W of

54 km S of Santo Domingo, Pair & Trainer 15836 (MO).

26. Dieffenbachia wendlandii Schott, Oesterr.

Bot. Z. 8: 179. 1858. TYPE: El Salvador. San-

ta Ana, H. Wendland s.n. (holotype, GOET!).
B.

Figures 26, 28

Stout herb, to (0.8)1.2-2(3) m tall; sap strong and
foul-scented (only weakly foul-scented in some At-
lantic slope populations); stems erect, decumbent
at base; internodes dark green to blackish green or
medium green, glossy to semiglossy, 1-5 cm long,
2-5.2
(averaging 25 cm long), matte, medium dark green,

cm diam.; petioles (11.5)16-32(65) cm long

sometimes finely darker green-striped throughout
(or at least near the base), often weakly glossy to-
ward the apex, moderately spongy, obtusely and
shallowly sulcate (sometimes more acutely sulcate
near the apex) to D-shaped, sometimes with a slen-
der erect margin or often terete in populations in
eastern Mexico, sheathed (0.3)0.5—0.9 their length;
sheath (6)12—30(45) cm long (averaging 18 cm
long); sheath sometimes markedly undulate on that
portion clasping stem, incurled throughout its
length with the margins incurled to erect and
touching or well-spaced, initially decurrent or near-
ly so at the apex and with one side completely hid-
ing the other from above the middle, sometimes
with the margins somewhat erect and eventually +
emarginate with one side rounded, the other side
rounded and somewhat free-ending, rarely with the
apex broadly rounded and free-ending; unsheathed
portion of petiole (1)3.5-12(24) em long (averaging
8 cm long), terete or thicker than broad, 12-14 mm
diam., 13-15

except terete in some areas on the Atlantic slope

mm thick, usually obtusely sulcate
of Mexico (the sulcus sometimes broader toward the
apex); blades narrowly ovate to ovate-elliptic,
(15)20—55(65) cm long, (9)10-22(28) cm wide (av-
eraging 35 X 17 cm), 1.3-2.4 times longer than
broad (averaging 2 times longer than broad), sub-
coriaceous lo moderately coriaceous, acute and
apiculate to abruptly or gradually acuminate al
apex (sometimes rounded and apiculate), acute to
obtuse or rounded and attenuate at base, sometimes
rounded to subcordate, slightly inequilateral, one
side 0.8—3.0(
surface dark green, semiglossy to weakly glossy.

4.5) em narrower than the other; upper

drying gray-green to yellow-brown; lower surface
paler, matte or nearly so, drying yellow-green to
yellow-brown (both surfaces dark yellow-brown on
very old specimens); midrib flat to broadly sunken

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

е,

pe К
es Hmm ;
EE

Figure 26. Dieffenbachia wendlandii. —A. Habit, plant with open inflorescence. —B. Adaxial blade surface, —С.
Potted flowering plant with open inflorescence (Croat 39749). —D. Open i ds нх 'ence at anthesis (Croat 47219). —
E. Staminate portion of spadix and spathe blade. —F. Close-up of spathe s E part of E portion, the mostly
sterile portion and the base of the staminate portion. A, B. (Croat 47219); D, F. (Croat 4721

760 Annals of the
Missouri Botanical Garden

86° 85° 84° 83° 82° 81° 80° 79°
78°
A
11° * . 11°
10° 10°
244
*
4 п P
i ^ =
y e D. aurantiaca \ 9°
HEUS 10 E
m D. crebripistillata *
E 6 ө * E & a
El D. fosteri E
** D. grayumiana
8° g y 8 ө 8°
A D. horichii |
A 100 0 100 Kilometers
— n
| | ' | 78°
86° 85° 84° 83° 82° 81° 80° 79°
84° 83° 82° 81° 80° 79° 78° 77°
A
11° N 44°
x N
A А
A
10° 10°
B
* "а"
9° 4 * 9°
% 3 B
a
ay | * Е "uL V
8° * D. burgeri à — а o м
El D. copensis C
= D. davidsei
7 4 D. hammelii »
* D. lutheri
6? 6?
B 100 0 100 Kilometers |
—..— | |
84” 83° 82° 81° 80° 79° 78° 77°
Figure 27. Distribution map. А. Dieffenbachia aurantiaca, D. crebripistillata, D. foste ri, D. grayumiana, and D.

horichii. —B. Dieffenbachia burgeri, D. copensis, D. davidsei, D. hammelii, and D. luth

Volume 91, Number 4 Croat 761
2004 Revision of Dieffenbachia
85° 84° 83° 82° 81 o 80° 79° 78° 77° 76°
11” 33:13
10°- -40*
9°- =9°
8°- . -Qo
€ D. concinna Ñ
ш D. fortunensis
* D. p а a
7°- А D. isthmia A T
A 100 0
І | | I | | 1 | | I
85* 84* 83° 82° 81° 80° 79° 78° 77° 76°
105° 100° 95° 90° 85° 80° 75° 70° 65°
15% 715°
10° 710°
5° -5°
El D. beachiana
9 D. killipii
A D. standleyi
ж x D. wendlandii Zo
0 Rs „ 0
В 300 0 300 Kilometers
5 | | 1 | | 1 | I | Р
105° 100° 95° 90° 85° 80° 75° 70° 65°
Distribution map. —A. Dieffenbachia concinna, D. fortunensis, D. galdamesiae, and D. isthmia. —B.

28.
i12 beachiana, D. killipii, D. standleyi, and D. wendlandii.

to flattened and concolorous to weakly paler above
with fine, close, slightly paler striations, convex to
round-raised or narrowly rounded and slightly to
moderately paler beneath, usually faintly striate
drying somewhat orange-tinged and paler than the

surface, 5—10(18) mm wide; primary lateral veins
(6)7 to 11(13) per side, weakly and obtusely quilt-
ed-sunken above,

convex, weakly pleated-raised
beneath, arising at an acute angle then spreading
at (40°)55°-70° angle, slightly paler than surface

762 Annals of the
Missouri Botanical Garden
99° 96° 93° 0° 87° 84° 81° 78° 75° 72°
c2
19” 219"
16° -16°
13°- -13°
* D. obscurinervia
e O. oerstedii
10°- 10°
200 0 200 Kilometers
۲ 7°
і | I I | | I I | |
99° 96° 93° 90° 87° 84° 81° 78° 75° 72°
89° 86° 83° 80° 77° 74° 71 °
8
10°- А Е -10°
y. Te
x O. longispatha
m D.pittieri
e D. tonduzii
4°- -4?
200 0 200 Kilometers
m B =4°
О g
" I 1 1 1 1 | І
89° 86° 83° 80° 77° 74° 71°

Figure 29. Distribution map. —A. Dieffenbachia obscurinervia and D. oerstedii. —B. Dieffenbachia longispatha, D.

pittieri, and D. tonduzii.

when fresh, usually drying darker than surface,
sometimes lighter than surface, moderately straight
or weakly curved to near the margin then gradually
curved upward along the margin to form a series of

closely parallel marginal veins that do not form a
collective; minor veins on lower surface moderately
obscure on fresh material, more prominent and

darker than surface on drying. INFLORESCENCE

Volume 91, Number 4
2004

Croat 763

Revision of Dieffenbachia

89°
12
N
9" ۸
6”
e D. nitidipetiolata
A D. panamensis
3*7
200 0 200 Kilometers
| | | |
89* 86° 83°
80° 75° 70° 65° 60° 55° 50° 45°
20°- E =20°
А є .
ә
e” ө А -15°
b.
e?
e D. seguine
10?7 740*
Kilometers
5°- 5°
0%, 70°
577 5°
I [| | ! 1 | ] |
80° Т5? 70° 65° 60° 55° 50° 45°
Figure 30. Distribution map. —A. Dieffenbachia nitidipetiolata and D. panamensis. —B. Dieffenbachia seguine.

l to 4 рег axil; bracteoles to 25 cm long; peduncle
(7)1 2-22 ст long, 1-1.5 em X 0.8-1.3 cm diam.,
subterete, pale medium green, weakly glossy, faint-
ly and finely striate-streaked; spathe (16)25-32 cm
long, narrowly acuminate to cuspidate-acuminate at
apex (the tip turned back), medium-green, weakly
glossy to semiglossy outside, equally colored and
glossy within with weak, darker, short oblique lines
arallel
throughout the length of the spathe: the spathe tube

running between the pa vertical veins

8-12 cm long, (2.7)3.5—4.5 cm diam. when furled,
6.5-12.5

nute depressions scattered throughout the tube:

cm wide when flattened, with dense mi-
constricted portion of spathe (2)3.3—4.0 cm wide,
3.5-8 cm wide when flattened; spathe blade 3.7—
4.5 cm wide, flattening to 3.3-6.3 cm wide: spadix
(12)18—29.3 ст long, 2.0—4.7 ст shorter than the
spathe, scarcely protruded forward, its stipe 1-2 cm
long, 1.3 cm diam.; the free portion of the spadix
9-11 cm long; pistillate portion (5.5)8.5-10 cm

Annals of the
Missouri Botanical Garden

long, 1.2-1.7 cm diam., 0.9-1.1 em on drying (ra-
chis 0.9-1.2 em diam.), the upper | cm sometimes
with as few as two apparently fertile flowers; sta-
minate portion of spadix (7)9-16 cm long, the fer-
tile staminate portion (4.5)7-12.5 cm long, gradu-
ally tapered toward both ends, (0.7)1-1.3 cm diam.
midway, 7 mm diam. 1 cm below the apex; mostly
sterile intermediate portion of spadix 2.0—4.0 cm
with a few aborted pistillate
half and a few sterile male

long, 7-9 mm diam.,
flowers in the lower
flowers in the apical half, often with a totally barren
segment of up to 1-2.8 cm long: pistils (33)45 to
55, depressed-globose, weakly pale vellow-green,
moderately glossy, (2)3 to 5 across the width of the
spadix, 3.0-3.7 1.5-1.7 mm high; stig-
ma yellow to pale orange, 0.6-1 mm high, 2.0-2.7

-

mm diam.,
mm diam., sometimes broadly sunken medially,
sometimes with a prominent, protruding dome held
slightly above the outer ring; staminodia 3 to 4, free
to the base, broadened toward the base, 0.8—1.2
mm wide at base and sometimes partly fused, usu-
ally slightly thicker near apex, (2.5)3.5—5 mm long,
white, slightly flattened, 1.5-3.5 mm wide, about as
long as the pistils; synandria 4 to 7 visible per spi-
ral, 3.5—4.0 mm diam., widely spaced at base, trun-
cate and smooth at apex, irregularly rounded, pale
tan, becoming bowl-shaped and brown except for
white, erect margins, margins sometimes crenate,
with thecae 6 to 8 per synandrium, these subglo-
bose, ca. 1 mm long, held just below the apex of
the synandrium. INFRUCTESCENCE with spathe
green at maturity; berries red to bright orange, 6—8
mm diam.
Distribution and habitat.
dlandii occurs principally in seasonally dry habi-
tats on the Pacific slope of Central America, rang-
ing from central Mexico (Oaxaca and Chiapas) to
Guatemala (Escuintla, Huehuetenango, San Mar-
cos, Suchitepéquez), El Salvador, Honduras (Mor-
Granada, Matagalpa, Nue-

Dieffenbachia wen-

azán), Nicaragua (Estelí,
va Segovia, Zelaya), Costa Rica (Puntarenas
Province), and Panama (Veraguas) at elevations of
75 to 900 m. In Mexico the species occurs on the
Atlantic slope only in the State of Oaxaca in the
Serranía de Juárez at 250-705 m and in Veracruz
Estación Biológica de Los Tuxtlas
The

in or near the
near the Caribbean coast at 5-165 m elevation.
only collection of the species in Panama, from Ba-
hía Honda in Veraguas Province, is unusual in hav-
ing blades more ovate and in ne pale green. It
may prove to be a new spec

Phenology. Dieffenbachia wendlandii flowers
principally in the rainy season, beginning in May
and especially in June and July, but continuing un-

til August or rarely September. What appears to be
a secondary flowering period may occur in the early
dry season because flowering collections have been
seen in December and February. Most fruiting
specimens have been made in the dry season and
early wet season from January to May.

Discussion. The species is characterized by its
robust, but moderately short stature, dark green,
semiglossy stems; narrowly ovate to ovate-elliptic
yellowish brown, to yellow-green-drying leaf
blades; but especially by the partially sheathed pet-
ioles with the sheath margins decurrent or ending
abruptly and rounded at apex with a free, un-
sheathed sulcate portion 1-9 ст long at the apex.
In addition, the species has an unusually large
spathe for the size of its leaves, frequently exceed-
ing 30 em long.

Populations of D. wendlandii on the Atlantic
slope have petioles completely terete, rather than
sulcate adaxially, but this varies even on the same
individual. In addition, these populations are more
ikely to have the petiole sheath even more decid-
edly decurrent at the apex. At least the populations
of plants in Oaxaca at middle elevation above Valle
Nacional have sap that is only mildly odorous,
whereas elsewhere the sap is malodorous, smelling
somewhat like skunk or peccary.

Dieffenbachia wendlandii is easily confused with
D. oerstedii on the eastern slopes of Chiapas and
Veracruz, but D. wendlandii is much more robust
than plants of D. oerstedii, which are usually less
than ] m tall and have internodes usually less than
2.5 cm in diameter. In contrast, the stems of D.
wendlandii are rarely less than 2.5 cm in diameter
and are usually 4—5 cm in diameter. Other differ-
ences in D. oerstedii are the sharply sulcate (rather
than terete to obtusely sulcate) petioles that are
white (rather than green) at the base, and the
sheath apex of which at least one margin is rounded
and prominently free-ending. In contrast, D. wen-
dlandii on the Atlantic slope is more than 1.5 m
tall at maturity, has internodes more than 3 em in
diameter, and petiole sheath margins acute to only
weakly protruded at apex with the free portion of
the petiole at most obtusely sulcate. Another way
D. wendlandii differs from D. oerstedii is by its typ-
ically larger spathe, over 25 cm long versus less
than 20 ст long for D. oerstedii

Previously most material of D. wendlandii from
Mexico and Guatemala has been mistakenly called
D. oerstedii, and indeed herbarium material without
good field notes is difficult to separate. Several of
the collections of D. oerstedii made in lowland Ve-
racruz (Holstein & Armbruster 20425; Nee 23773.
29752, and 29993) appear have the petiole

Volume 91, Number 4
2004

Croat 765
Revision of Dieffenbachia

sheath somewhat decurrent without a conspicuous
free-ending apex. They are described as plants no
more than | m tall. It is possible that these rep-
resent hybrid plants since both D. wendlandii and
D. oerstedii occur in lowland Veracruz.
Dieffenbachia wendlandii has been confused
with D. standleyi in eastern. Nicaragua. However,
that species occurs only on the Atlantic slope and
has petioles sheathed completely to the apex and a
proportionately longer blade, ranging from 1.9 to
3.5 times longer than wide, and averaging 2.5 times
longer than wide. In contrast, D. wendlandii has
blades ranging from 1.3 to 2.4 times longer than
wide and averages only 2 times longer than wide.
Throughout its range in western Mexico and Central
America, D.
shape with the proportionately broader blades oc-

wendlandii is variable in the blade
curring in Mexico and Guatemala, where they av-
erage 1.8 times longer than wide. The collections
from El Salvador and Nicaragua, on the other hand,
have leaf blades averaging 2.3 times longer than
wide. The populations in Mexico and Guatemala
have shorter petioles (averaging 19.8 cm long and
22.6 cm long. respectively) than those in El Sal-
vador and Nicaragua (averaging almost 30 ст
long).

The single Costa Rican collection made in Pun-
tarenas Province, along the dry road approaching
the Monteverde reserve, is noteworthy in being so
far out of the range of the species. Dieffenbachia
wendlandii may have been more widespread in
Costa Rica,
country have been eliminated between the Montev-

but much of the drier forests in the

erde site and the Nicaraguan border.

Stevens 6027 from Matagalpa Department, Nic-
aragua, at 910 m is unusual in having the apex of
the petiole sheath broad and conspicuously round-
ed and somewhat free-ending. It may ultimately
prove to be a different species.

While many specimens of D. wendlandii in Mex-
ico and Guatemala have blades that are subcordate
at the base, most collections in El Salvador and
Nicaragua have leaf bases attenuate at the base.

Engler (1915), in his revision of Philodendroi-
deae—Dieffenbachieae, considered D. wendlandii a
synonym of Dieffenbachia seguine var. viridis Engl..
one of many varieties of what he considered a poly-
morphic species ranging throughout Central Amer-
ica, the West Indies, and South America. In my
opinion, Engler misinterpreted the Central Ameri-
can material, much the same as later botanists, in-
cluding myself, did for years. However, after actu-
ally seeing the live plants in the field їп both

entral America and in the West Indies, there is
no doubt that D. seguine does not occur in Central

America. The material previously determined as D.
seguine in Central America has proven to be either
D. oerstedii with blades larger than normal, or D.
wendlandii.

COSTA RICA. Ala-

Additional елү examined.
juela: Río
Puntarenas: p to Monteverde,
(DUKE). EL SALVADOR. Wendland 410 (СОЕТ); San
0 Calderon 914 (US), ied uc (NY, US). GUA-
er he pue Engler 2. Н Escuintla-Alo-
tenango, mi. 6, Croat 42050 1 M Q): Cucunya at
San D бай Seler 2389 (С), Seler 2398 (GH). Hue-
huetenango: Cerro Victoria, Finca San Rafael, Sierra de
los Cuchumatanes, Steyermark 49637 (F). San Marcos:
Finca Armenia near La Trinidad above San Rafael, Croat
40790 (ENCB, MO): Río Ixpal. below Rodeo, Standley
66724 (F); Santa Rosa, о El Ahumado, N of
Standley > of Cuilapa, Standley
Maza pareve ora 1047
А ‚ MO). HON-
DURAS. Francisco _ жы 5ап Anni e г nte
. Standley 21077 (F). .€ hia-
» Ovando, 2.8 km МГА Tarquin
Croat 47510 (MO); Escuintla- El Triunfo, ca. | mi. N of
Escuintla, Croat 43813 (MO); ere hula-Nueva Aleman,
mi. 4, Croat 43791 (CHIP, CM, : Mapaste 4 . Sierra
de Soconusco, Croat & D. Hannon p О); Tapachu-
la-Union Juarez, at km 13.5, 1.3 mi. N of Trinidad, Croat
47219 (CHIP, MEXU, MO); Acacoyagua, Ejida Las Go-
landrinas, Cerro Mt. Ovando Trail, Croat 78480 (MO):
Aci HON R. Hernández 473 us XU. MO, NY); Es-
cuintla, Esperanza, Matuda 16765 (F. MEXU); Lape ranza,
eae 16369 ж Оахаса: nae spec, 6 mi. W of
alle Nac. on 8 5 5, Croat 39749 (AAU. MEXU. MO,
nd SEL. 15 ‘Us VEN), Croat 43931 (MEXU,
MO), pA E i Hannon 65536 (MEXU. MO). Croat
O). с 78720 (МО); Sta. Maria Chimalpa,
Hernández 1318 (MO): Arroyo Sangre, ca. 1-2 km al I
de Sta. Maria, ин в 2586 МО). Queretaro: Huim-
Прап. Mpio. Comaltepec, Puesto nn Lopez Garcia &
Martin 122 (MO, CR). Veraer 9.3 mi. from Tabasco/
Veracruz de т on Hwy. 180 to 5 Thompson

Los Cerritos,

=

`
©
N
—
—

MO): San Andres Tuxtla, Catemaco-Montepio, 22.2
km N of бае о. vic. Est. Biol. Los с Croat &
U, MO), б. K. Martínez 2287 (F,

M. Pérez 78686 (MEX
MEXU, NY); Catemaco, NUR arroyo Basuras,
R. Perminas 645 (F, MEXU, E US). NICARAG
elí-La Conc ordia, km | i

МО); 2 km al SE de |
16164 ( (MO), Sandino 1248 (MO); 1 km SE of Cutirre.
Moreno & Henrich 8427 (MO). Managua: Garnier 772

(US). Matag alpa: Hwy. 5 ca. 38.7 km from Hwy. 3 inter-
section, ca. 5.5 km N of Río Tuma das, Stevens 6027
(DUKE, MEXU, MO). Nueva Segovi 1.6 km W of
Murra-El Jícaro, km 1, Quebrada El (mel "n, Stevens et
al. 17591 (MO); Río Solonli, Quebrada por 3 km S
of Jalapa, 6 Apr. 1977, Neill 4657 (MO). ANAMA. Ver-

aguas: Sond, Bahía Honda, 7°58’, 81° on Ibáñez et al.
(PMA).

1829
EXCLUDED SPECIES

Dieffenbachia lancifolia Linden € André, placed
in synonymy of D. seguine by Engler (1915); how-

766

Annals of th
Missouri cabal Garden

ever, this is a distinet species from Antioquia De-
partment, Colombia.

Dieffenbachia picta Schott forma lancifolia (Lin-
den & André) Engl. and Dieffenbachia picta Schott
subvar. lancifolia (Linden & André) Engl. are com-
binations of Dieffenbachia lancifolia Linden & An-
dré that also must be excluded from consideration
in this revision of Central American Dieffenbachia.

Dieffenbachia meleagris Linden & Rodigas,
placed in synonymy of D. seguine by Engler (1915);
however, this is a distinct species from Ecuador,
possibly one synonymous with D. spruceana Schott.
The recombined Dieffenbachia meleagris Linden &
Rodigas subvar. meleagris is also to be excluded.

Dieffenbachia shuttleworthiana Engl. was syn-
i . picta by Engler (1915), but it
must be excluded along with the combination

onymized with

D. picta Schott forma schuttleworthiana (ege
Engl. and D. shuttleworthiana Hort. Bull. This
ombian species is not closely related to D. seguine.

SPECIES INCERTAE SEDIS

The following species names are believed to be
synonyms of Dieffenbachia seguine based on the re-
vision of Dieffenbachia by Engler (1915); however,
owing to the destruction of many herbarium spec-
imens during World W
impossible. The specimens were no doubt available

Jar II. lectotypification was

during Engler’s time, and it is assumed that he saw
the material.

Dieffenbachia picta fo. mirabilis Engl., Fl. Bras.
3(2): 176. 1878. TYPE:

unknown origin cultivated by Verschaffelt, not

based on a plant of

designated. No type listed by Engler.
Dieffenbac hia seguine fo. decora Engl., Fl. Bras.
3(2): 175. 1878. Dieffenbachia seguine subvar.

Bot. Jahrb. Syst. 26: 568.
1899. Dieffenbachia seguine var. decora (Engl.)
Engl., Pflanzenr. IV. 23 Dc(Heft 64): 47. 1915.
Dieffenbachia seguine fo. decora (Engl.) Engl..
Pflanzenr. IV, 23 Dc(Heft 64): 48. 1915, nom.
superfl. Dieffenbachia decora Hort. Versch. ex
Engl., in DC., Phan. 2: 446. 1878.
TYPE: based on a plant of unknown origin
cultivated by Verschaffelt, not designated. No

decora (Engl.) Engl.,

Monogr.

type listed by Engler.

Dieffenbachia seguine fo. nobilis Engl., Fl. Bras.

3(2): 174. 1878. Dieffenbachia sei s г.
nobilis, Bot. Jahrb. Syst. 26: 568. 1899. Dief-
fenbachia seguine var. nobilis сен En gl.,
Pflanzenr. IV 23 De(Heft 64): 47. 1915. TYPE:
Brazil. Pará: Barraquin based on a cultivated
plant by Verschaffelt. No type listed by Engler.

Dieffenbachia picta subvar. 5 Engl., Bot.
Jahrb. Syst. 26: 569. 1899.
cultivated plant of ш origin, not seen.

YPE: based on a

No type listed by Engler.

Dieffenbachia seguine var. minor Engl., Bot. Jahrb.
Syst. 26: 567. 1899. TYPE: No type listed by
Engler.

Dieffenbachia picta var. latior Engl., Bot. Jahrb.
Syst. 26: 569. 1899, TYPE: No type listed by
Engler.

Dieffenbachia picta var. latior Engl., Bot. Jahrb. 26.
569. 1899. TYPE: Not seen. No type listed by
Engler.

Dieffenbachia picta subvar. memoria Engl.,
Jahrb. Syst. 26: 570. 1899, TYPE:

living material at 2 Botanical Garden

Bot.

based on
ж Buitenzorg), not seen. No type listed by

gler.
Pec picta subvar. mirabilis Engl., Bot.
ahrb. Syst. 26: 570. 1899, Dieffenbachia mir-
in DC., Monogr. Phan.
based on a cultivated

abilis Versch. ex Engl., i
2: 448. 1878. TYPE:
plant of unknown origin by Verschaffelt, not
seen. No type listed by Engler.

Dieffenbachia picta var. angustior Engl., Bot. Jahrb.
Syst. 26. 569. 1899. TYPE: No type or locality
listed, not seen. No type listed by Engler.

Dieffenbachia seguine fo. viridis Engl., Fl. Bras.
3(2): 174. 1878. Dieffenbachia seguine subvar.
viridis Engl., Bot. Jahrb. Syst. :

Dieffenbachia seguine var. viridis Engl., Pflan-
zenr. IV. 23 Dc(Heft 64): 45. 1915. TYPE: Not
seen. No type listed by Engler.

Dieffenbachia seguine var. lineata (K. Koch & Bou-
ché) forma? decora (Engl.) Engl., Pflanzenr. IV.
23 De(Heft 64): 48. 19
guine var. decora (Engl.) Engl.,
23 Dc(Heft 64): 47. 1915. TYPE: based on à
cultivated plant of unknown origin by Ver-
schaffelt, not seen. No type listed by Engler.

Dieffenbachia picta var. typica Engl., Pflanzenr. IV.

3 Dc 50. Fig. 21. 1915. TYPE: cultivated in
European gardens. No type listed by Engler.

Literature Cited

Barabé, D., A. Bruneau, F. Fore Lacroix. 2002.
The corre lan Б По of atypical bisex-
ual ае and кунш in the Aroideae (Araceae).
Pl. Syst. Evo X : 1-19.

Berlin, B. & P. i Basic Color Terms, Their Uni-
хован апа сл Univ. California Press, Berke-
ley

Bogner H. & D. H. Nicolson. 1991. A revised classifi-

ion of Araceae with dichotomous keys. Willdenowia
21. 35-50.
Bunting, С. S. 1963. New species of Araceae from Chi-

Volume 91, Number 4

Croat
Revision of Dieffenbachia

manta Massif, Gran = Venezuela. Bot. Soc. Venez.
Ci. Nat. d
LC i on Mexican Araceae. Gentes

Не. $ E —:
79. Тр sinopsis de las Araceae © Venezuela.
Agric. (Maracay) 10: 139-29
Notes on a Guayana Die hai (Ara-
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APPENDIX 1
LIST OF SPECIES.

. Dieffenbachia aurantiaca Engl.
. D. beachiana Croat & Grayum
ч D. burgeri Croat & Grayum
. D. concinna Croat & Grayum
. D. copensis Croat

їл =

. crebripistillata Croat

. davidsei Croat & Grayum
8. D. fortunensis Croat

. fosteri Croat

. galdamesiae Croat

11. D. grayumiana Croat

. hammelii Croat & Grayum
: horichüi C гоа! & Grayum

A longi Engl. & K. Krause

7. D. lutheri Croa
183. D. nitdipetiolata Croat
19. D. obscurinervia Croat

. oerstedii Schott

21. D. panamensis Croat
22. D. pittieri Engl.

. seguine (Jac d ) Schott

25. D.t
26. D.

nduzii Croat & Grayum
Menta Schott

APPENDIX 2

INDEX TO EXSICCATAE. TYPE SPECIES IN BOLDFACE
Acevedo-Rodríguez 4705 (23); Acosta Solís, M. 10896
(15); Aguilar, R. 256 (20), 2195 (4), 2380 (20), 2412 (20),
5204 Са Aguilar et al. 4302 (20); Akers,
78A (11); Allen 5669 (4), 5669A (4), 5972
Mo 1839 (6); Alvarez, A. & Р. Herrera 699 (15); Al-
a et al. 283 (19), 376 (15); Anaya ! (20); André 1202
( 23), 7 (15); Antonio den (2: >), cae (6), 3820 (6),
4488 Ga 4546 (14), 4638 (15), 226 (15); Antonio &
Hahn 4405 (15). 4406 T Nane et ab 2860 (20); Ar-

cher 2215 (19); Aristeguieta 1764 (23); Asplund 1557:

(15); Atha & Zanoni 770 (23); Atwood 212 (26); Augo
1693 (23): Aymard & Ortega 3090 (23); Aymard et al.

2114 (23).

Bailey 335 (14); Baker & Burger 90 (25); Balick et al.
1738 (20). 2080 (20). 2359 (23). 2716 (20); Barfod &
Skov 60101 (18); Barfod et al. 48154 (18), 48348 (18);
d 8. E (20); Barringer 1790B (13), 2416 (18), 2432
(11), 3525 (25); Barringer et al. 1973 (4), 3479 (25), 4039
(25), 15 (20); Bartlett & Gentry 7423 (15); Bay 278
(15); Beach 1429 (20), о (20), 1431 (20). 1432 (20).
1433 (20), 1434 (20), 1435 (20), 1436 (18), 1439 (18),
1440 (11), 1441 (11), 1448 (2), 1485 (2), 1518 (20); Beard
656 (23); Beck 17103 (23); Beck et al. 295 (23); Bello &
Cruz 4284 (20); Bello et al. 42 (20); Benftez de W et
al. 4661 (23); Bernal et al. 1158 (19); Betancur et al.

(18), 3054 (25); Beutelspacher s.n. (20); Bill iet As Ja
7346 (23), 7347 (23), 7357 (23), 7 23);
| 23); Blackmore & Chorley i | n
Blackwell et al. 2704 (18); Blum & Tyson 2324 (15): Bog-
ner 965 (23); Bourgeau s.n. (20); Brand & Ascanio 277
(14); Bravo 31 (20); Bravo s.n. (MEXU 30199) (20); Bravo
& Nu 107 (20); Breedlove 12752 (20). 24166 (20), 33839
(20), 34977 (20), 40155 (20); Breedlove & McClintock
34192 (20); Breedlove & Thorne 30681 (20); Britton 447
(23), 4126 (23); Britton & Britton 7897 (23), 9664 (23).
10082 (23); Britton & Shafer 1625 (23); Bunting 1692
(23), 2026A (23), 2027 (23), 2035 (23), 2036 (23), 2044.
(23), 2622 (23), 2678 (23), 2729 (23), 2738 (23), 2829
(23), 3321 (23), 11687 (23), 13515 (23); Bunting & Fer-
nandez 3295 (23); Bunting & Holmquist 4319 (23);
ting & Manara 2119 (23), 2120 (23), 2122 (23), 2123 (23),
2124 (23), 2124V (23), 2125 (23), 2126 (23), 2127 (23):

=
=
mc
On
N
л
eJ

Volume 91, Number 4
2004

Croat
Revision of Dieffenbachia

—

Bunting & Trujillo 2236 (23); Bunting et al. 1937A (23),
1949A 8 1997 (23), 2072 (23), mage (23), 2073 (23),
4108 (23); Burch et al. 112: ; Burger & Antonio
10905 (1 "3 11198 (18). 11224 (15), 11249 (4); Burger &
Baker 9968 (11). 10121 (3), 10137 (13); Burger & Gentry
Jr. 8898 (3); Burger & Liesner 7111 (20), 7196 (4), 7254
(3); Burger € Matta 4181 (11); Burger & Pohl 7825 (20):
Burger & Stolze 5024 (18), 5461 (4), 5489 (3), 5753 (18),
5754 (2); Burger et al. 1323 (20), 10323 (18), 10669 (13),
10671 (3), 10699 (18), 10734 (11), 11695 (20). 11926
(20); Busey 743 (1).
Cadet 6030 (23):
ES 2092 (25); Callejas б. al. 4873 (19),
25): Calzada 338 (20); Camp E-3599 (15), 3653 (15):
Carballo et al. 47 (20); Carleton 508 (20); Carlson 153
20); Carrasquilla 2005 (18); Carrasquilla & Me du
1239 (18); Carrasquilla & Rincón 304 (15): gio
(20); Catharino et al. 1909 (2: 3); Cedillo, T. 3645 s
Cerón & J. Corozo 33858 (18), 33947 "t 34097 (18):
Cerón et al. 29159 (15); Chacón 364 о, 507 (11). 5
(12), 1406 (13); Chacón et al. ; Chavarría К
Umaña 157 (13); Chavarría et al. 8 Chazaro 416
(20); Chinchilla 137 (20): al & Churchill 6105
(18), 6158 (8), 6159 (8), 6252 (25); Churchill & de Nevers
4333 (15); Churchill et al. 3993 (6), 4032 (15), 4125 (15):
Clarke 60 (20); Clewell & Tyson 3306 (15): Clezio 221
(15); Cogollo et al. 3462 (25); Cole xy? үзү (23); Соп-
гай & Conrad 2882 (20); Conrad et al. 2
& Bonifaz 3107 (15), 4195 (15), 4
5210 (15); Correa & Montenegro
Cowan 2063 (20); Cowell 550 (23):
mers 9896 (23): и 4095 (16),
4), 5259 (16), 5:
5761 e 5767 (16), 58
6192 (16), 6276 06) 6308 (14), ‚ 6471 (16).
6502 (14), 6775 (19), 7136 (16). 7455 (16). 7478 (6).
7712 (14), 8623 (19), 10133 (14), 10982 (14), 11291 (14).
. 11411 (16), 11420 (6). 11514 (16). 11570
5). . 12123 (6), 12229 (16), 12319 (16).
123524 (19). 12353 (15). 12401 (15). 12489 (15). 12491
(15). 12660 (19), 13403 (6), 13849 (19), 14175 (6), 14309
504 (15), 14706 (15),

T

Calderon 914 (26); Callejas & Jan-
5661 (18), 9704

. 10647 (6):
Cowgill 532 (23): Cre-
4125 10), 1134 (16),
. 0409 (14),
. 5896 (14),

. 17210 (6). 17311 (15).
(1). 21999 (20). 22173
(20). 22252 (20). 24250 (20), 25213 (6), 25352 (6). 20193
(6), 26239 (6), 27161 (18), 27196 (16). 27206 (21). 27490
(25), 32955 (1). 33018 (16), 33551 (15), 33568 (6), 31442
(15), 34475 (14), 34654 (16), 34656 (14), 34745 (14).
35079 (1), 35108 (4), 35206 (20). 35210 (1). 35292 (1).
) ‚ 35702 (4), 3575(25), 35915 (О),
36297 (20). 36444 (20). 30472
А 36747 (25). 36821 (25).
37351 (20). 37361
37605 (15). 37746 (18).
38229 (18). 38344
(15). 39749 (26), 40062 (20).
40107 (20). 40103 (20), 40790
20), 42556 (24),
43217
33: 20), 13308 (18),
43629 (25), 13791 (26). 43813 (26). 43931 (26). 44226
(11), 44246 (20), 44254 (18), 44283 (2). 44307 (18).
44317 (25), 44321 (11), 44558 (6), 44682 (6), 46785 (20),
46945 (25), 46947 (18), 47088 (5), 47219 (26). 47510
(26), 47868 (20), 48437 (15), 48672 (8), 48778 (25).
48816 (15), 48903 (25), 49056 (15), 49070 (25), 49124

37479 (15).
‚ 38120 (18),
. 38069 (1: 5), 38047
7 (20), 40089 (20),

(10), 49155 (6), = (6), 49310 (25), 49761 (18), 49708
18), 49791 (19), 49805 (15). 49932 (25). 49971 (8).
50049 (2: 2 50480 Ks 50055 As 5). 50684 (15), 50725
(15). 52300 (25). 537 92] (23). 53956 (23).
54380 23, 54649 [X 5). 55629 (15). 55606
. 96205 s :
7427 (25). 57462 (18). +
(2). 60567. (23), 60613 ез 60807 23. 62831 "En
66533 (25). 60732 (25). vat (8), 00953 (2), 60993 (25),
07115 (6), 61197 (15), 6 1329 9), 67379 A (18), 67399A
‚ 617533 (20), 67576 (6),

). 67692 (3), 67700 (1), 07837 (8), 68012 (8),
68069 (20), 68097 (25). 68195 (18). 68196 (25). 68336

—

(25), 68358 (2), 68359 (11), 68379 (18), 68449 (20),
08494 23). 68547A (23), 68582 (23), 68679 (15), 68699
(6), 68746 (6), 68820 (21), 68854 (18). 68961 (15).

68971 m 69070 n 69343 (15), 70099 (25), 70868
(25), 71017 (25), 71119 (15),

(15),
74801 (6).
(11), 74958 (18),
15149 (19). 76154 (15),
(4), 77283 (20),
(23). 78345 (23),
78695 (20), 78711 (26),
(4), 78733 (11), 78758 (12 *
(25), 187 88 (18), 78830 (20),
79072 (20). 79073 (13).
А 20329 (15), 19: 348 (18), 79359 (15),

74930 (25).
15007 ü 7),
7517 72 ( 0.

78480 (26). 78078 20). 78687 (20).
78720 (26), 78731 (12), 78732
78771 (2), 78784 (20), 78787
78838 (25), 78859 20),
79075 (20), 7
82829 (15 5).

—

75707 nt 5) eat & Cogollo 52174
Gaskin 80391 (25); Croat & \
(4), 59814 (3). 59851 (3), 59906 (J). 59929 (20), 60002
(8), 60070 (25), 60112 (25). 60116 (18), 60130 (2).
60139 (25), 60149 (11), 60255 (2), 60346 (8), 60355 (25):
Croat & D. Hannon 63129 (20), 63167 (20). 63340 (26).
64109 (24), 64317 (24), 64476 (24), 61622 (20). 64638
(24), 65370 (20), 65536 (26), 74856 (21), 79112 (3),
79115 (13), 79167 i 79170 (4), 79191 (4), 79193
(1), 79199 (18), 79211 (3), 79238 (4), 79284 (20).
79286 (3). 79291 (4); (od & M. Mora 83652 (18), 83085
(7). 83096 (25). 83777 (16); Croat & Nuñez 82004 (1 0
Croat & M. Pérez 78686 (26); Croat & Porter 16249 (25

16303 (18). 16375 (18). 16412 (18). 16499 (11): Croat ^
Zhu 10203 (16). 76253 (15). 76254 (18). 70250 (16).
. 76259 (15). 76266 (16). 76328 (25),
(8). 76422 (18). 76449 (18), 76482 (18),
70500 (10), 76597 (7). 76044 (6), 76653 (25 53.
(15), 70000 A (19), 70746 (15), 70757 (6), 7
76858 (25). 76859 (20), 76942 (18), 77017 (7),
У 0042 (16). 77048 (15), 77101 (16). 77102 (15),
(14), 77201 (20); Croat et al. 82305 (25). 82441
(25). Ae 20 (18), 83795 (15), 83804 (15), 84041 (18);
Cruz 354 (20); Cuatrecasas 4225 (23). 15053 (25).

Y Arey 769 (23), 770 (23), 9420 (15). 9678 (6), 10766
(20); D'Arcy & Sytsma 14498 (15); Davidse 35802 (20):
Davidse & Brant 31879 (20), 32366 (20), 32410 (20);
Davidse & D'Arcy 10098 (15); Davidse & González 13410
(23), 21012 (23); Davidse & Hamilton 23599 (15), 23017
(7): Davidse & Herrera 26262 (20). 31077 (12), 31154
(12). 31213 (11); Davidse & Holland gue (20); Davidse
& Holst 36041 (20); Davidse et al. : :
20326 (20), 20440 (20). 20914 чя 20510 (20).
(20), 35484 (24); Davidson 7164 (20); de Nevers К! н.
Herrera 3975 (7), 5898 (18); de Nevers et al. 4709 (7),

770

Annals of the
Missouri Botanical Garden

5727 (18), 7407 (18), 7409 (19), 8267 (15); Delinks 452
(15); Dillon et al. 1837 (20); Dodge 10020 (4), 10198 (4);
Dodge & Goerger 9489 (25), 10157 (20); Dodson 6188
(15); Dodson & Dodson 11130 (15); Dodson & Tan 5338
(15); Dodson et al. 8415 (15), 10594 (15), 14638 (15);
Donnell Smith 7813 (20); Drake 7 (23); Dressler 4688
1716 (14), 5316 (10); Dryer 1681 (11);
(14), 5099 (15), 5169 (15), 5260 (15), 5437 (15), 13082
(15), 13601 (15), 14346 (15), 15591 (15); i
bride 14019 (15); Duss, P. 3790 (23), 21496 (23); Dwyer
2077 (15), 4565 (15), 9920 (20), 11184 (20); Dwyer &
Diec Eun v 3008 (20); Dwyer & Gentry 9479 (6

Eggers 14183 (15), 15095 (15); Ekman 1983 (2: 3); En-
gler 226 22 227 (23), 2389 (26), 2793 (23); Espina et
al. 2902 (15); Espinosa & ran 3 (45), 3939 п
Espinosa & E. Martínez 3308 (6); Espinosa et al.

(15), 3611 (15), 4478 (15), 4723 (б), 10035 (20).

Faden et al. 76/82 (20); Fallen & Ray 860 (15); Fish-
lock 326 (23); Folsom 1265 (6), 1444 (15), 3211 (6), 4054.
(20), 6218 (6), 6247 (15), 8712 (20), 9200 (18), 9329 (12),
9724 (11), 10116 (25); Folsom & Collins 436 (15), 6486
(21); Folsom & Mauseth 7844 (15); Folsom et al. 2111
( 5), 6852 (15), 8264 (21); Fonnegra 1344
25); Fonnegra et al. 2899 (18), 2907 (18); Forero 719
5); Forero et al. 1723 (14), 4571 (18), 4659 (18), 6272
5), 6489 3 17 00 (15), 9047 (15); pres 10213 (20
14); Foster et al. 14649 (9); Fuentes
0 (20): сы s 564 (23); Funk et al. е (25), 10718

25).

—

—
nn

Galdames Т al. 1138 (18), 1330 (7), 1570 (7), 1626
(14), 2252 (14), 2286 (14), 2486 (14); Galeano, G. 4600
(25); Galeano, G. et al. 4825 (19); Gamboa et al. 71 (1:
91 (1 pe Garibaldi 68 (14); Garnier 772 (26); Gentry 3035
(25), 26705 (25); Gentry & Dwyer 3643 (15); Gentry &
Forero pos (18). 7342 (18); Gentry & Juncosa 41037
(18); Gentry & Lajones 73108 (15); Gentry & Tyson 1653
(14); Gentry et al. 3406 (15), 24700 (25), 26709 (15),
28574 (14), 72496 (15), 72955 (25), 75903 (25); Gomez
19038 (20), 19531 (4), 19532 (20), 19572 лан 20562А
(20), 20565 (20), 22016 (20), 22951 (13); €
rera 23477 (25); Gómez et al. 20405 (2: 5). 2 108 (20);
;ómez-Laurito 7792 (1: 3), 7850 (4); Gómez-Pompa 1505
23); González 1473 (20), 6711
(20), 3341 (20), 5 5597 (20); Gordon 55С (18), 339 (25);
Grant & Кипде 92-01928 (4); Grayum 2225 (18), 2288
(11), 2771 (20), 2772 (12), 2780 (25), 2840 (4), 4756 (13),
4765 (20), 6194 (20), 6887 (11), 6899 (2), 6918 (20),
6925 (20), 6936 (2), ео (12), 7698 (2), 8638 (13),
9251 (20), 9277 (20), 9773 (11), 9777 (4), 9804 (25),
9830 (11), 9844 (18), б (4), 10858 (25); Grayum &
Evans 10156 (4); Grayum & Fleming 8119 (4); G
& Hammel 5785 (18); Grayum & G. Herrera 7829 (20),
9139 (1), 9236 (3); ا‎ & Jacobs 3524 (18); Grayum
& Murakami 9939 (25); ( hatz 3174 (25),
3206 (11), 3218 (18), 3220 (2), 5279 (25); Grayum &
Sleeper 6100 (20); Grayum & Warner 5710 (20); Grayum
et al. 3982 (4), 3983 (4), 4014 (3), 4440 (7), 4447 (4)
4483 (7), 4961 (20), 5467 (13), 5719 (20), 5723 (13),
5862 (20), 7547 (3), 7549 (1), 7567 (4), 7657 (15), 8038
(11), 8336 (13), 8345 (20), 9250 (4), 9469 (25), 9744 (12).
9962 (4), 9973 (23), 10578 (20), 11116 (11), 11139 (4),
11163 (11), 11169 (12), 11174 (13); Grove 01 (20); Guer-
ra & Liesner 287 Guillermo, J A D. Cardenas L.
863 (16); Gutierrez, G. & Barkley 171 25).

Haber & Atwood 9163 (20); Haber E "Bello 7191 (20);
Haber & Hammel 1799 (20); Haber & Zuchowski 9251
(20), 11175 (25); Haber et al. 4979 (20), 10824 (25);

D

— —

Hahn 142 (15), 945 (23); Hammel 122 (2). 778 (21), 3140
(6), 3586 (20), 3781 (6), 4049 (18), 4101 (20), 4298 (14),
4484 (19), Vieh (14), 5607 (7), 6264 (20), 7212 (6), 8123
(18), 8167 (11), 8212 (12), 8270 (20), 8273 (12), 8415
(20), 8606 (20). 8617 (11), 8748 (12), 8784 (4), 8846 (2),
8 4 (25), 9688 ( 2 (4), 9922 (20),
10081 (4), 10082 (18), 10449 (20), 12320 des
(5), 13685 (7), 20231 (20); Hammel & D'Ar
Hammel & Grayum 14169 (1); Hammel & Au
2 (20), 14211 En
(14), 14786 (19), 15836 (25); Hammel et al. Я
, 14472 (15), 16262 (14), 16397 (7), т (25),
20114 (20); Harling 313 (15); Harling & Andersson
16727 (15), 18898 (15), 19371 (15), 24778 (15); Harmon
& Dwyer 4035 n Harmon & Fuentes E 10 (20), 6419
(20); Harris 8361 (23); Harris & Neal s.n. (23); judge
R. 12488 (15); Henny 5 d (23); Herbst & S. Ishikaw
5459 (23); Heredia, M. 60 (23); Hernández 473 (26), 542
(20), 605 (20), 1318 (26), 2586 (26); Hernández & Vaz-
quez 551A (20); Herrera 1636 (20), 4116 (18); Herrera,
G. et al. 2928 (20); 5 H. 245 (19); Heyde & Lux
4654 (20); Higgins, J. 119 (23); Hill, S. 24812 (23);
Hitchcock s.n. (23); e 2929 (23); Hodge & Hodge
3174 (23); Holm-Nielsen et al. 2769 (15), 25355 (18);
Holst 62370 (23); Holstein & а 20425 (20);
Hoover 1324 (15); ipid et al. 3161 (25), 3968 (25);
Horich s.n. (11), s 1 11564 (23), 11744
E mi Howard & Nevling 16978 (23); Huft & Jacobs 1997

—
—

jm 167 (20), 455 (20), 645 (20); Ibáñez et al. 1829
(26); Ibarra & Cedillo. 1804. (20); Iltis et al. 30338 (20);
INBio 186 (20); Ingram 1124 (15), 1146 (17), 1169 (23),
16452 (25).

Jacobs 2159 (20); и 103 (18), VI (18); иа
. 2 5 (14); Johnston, J. R. 305 (23). Judd et al. s.r
; Juncosa 619 (25), b, (1 5), 1795 (18), 1898 (18),
io (18); Jones, A. & Tejada 275 (15

Kennedy 455 (15), 1193 (14), 1594 (15), 2661 (15).
3253 (25); eae & Foster 395 (15); Kennedy & Sol-
omon 4629 (20); 5 Чч 4); Кегпап 381 (20), 748

Kernan & Phillips 831 (4); Kew 70-76-494 (20); Kil-
lip 12154 (15), 35113 TES 39979 (14); Knapp 1042 (19),
2165 (4), 2275 EM 5758 (6); Knapp & Mallet 3089 (15);
ae et al. 1717 (6); Koshear 59 (4); Kress 77-830 (15
1 (15), a 630 (25), 84-1622 (20), 84-1632 (11);
Kuler J. 394 (20); Kursar & Coley 4 (15); Kvist & Asanza
40756 (18); Kvist et al. 48348 (18).
Las 16678 (15); Lavastre 1845 (23); Lazor & Tyson

2 (15); Lazor et al. 2578 (18); LeClezio 135a (16); Le
сой A. 95 (23); Lehmann s.n. (15), 5311 (15), 8876 605

eija & Garza 3341 (20), 5597 (20); Leimbeck, R.
7 Lent 37 (18), 161 (1), 639 (25), 694 (25), 2789 ч
4042 (25); Lent et al. 3374 (18), Leon 720 (25), 26573
(25); Lewis et al. 1753 (6), 2195 (14), 3251 (14); Liesner
114 (1), 1736 (3), 2871 (4), 14102 (20), 14394 (25); Lies-
ner & A. González 10126 (23); Liesner & Judziewicz
14797 (25); Liesner & Mejía 26236 (20); Liesner et al.
7681 (23). 15035 (20), 15122 (20), 15144 (18), 15330
(25), 15365 (25); Liogier 13307 (23); Liogier & Liogier
20185 (23); Lister & Colchester 272 (23); Lloyd 237 (23);
Loiselle 106 (25); (20); Løjtnant & Molau 15839 (15);
Lopez Garcia & Martin 122 (26); Lotto s.n. (23); Luteyn
1010 (6), 1203 (15), 3175 (15), rea (15), 3188 (6), 3263
(20), 3342 (20), 3385 (18), 4043 (14); Luteyn & Croat
)6 (14); Luteyn & Kennedy 1255 (6), 1837 (6); Luteyn
& Wilbur 4569 (20); Luther s.n. (23).

Maas et al. 7834 (1); MacDougal 1027 (18), 1090 (20),

ә
T

جر

Бе
S

ке,
=

Volume 91, Number 4

Croat
Revision of Dieffenbachia

3193 (20), vue 20), 3303 (24); Matic 589 (20), 627
2 (20); Madison et al. 15); Me-
MS (23); Marten beu ), bn 0 848 (3
í x MNT 13 (20), 23175
: . E. 2287 (26),
13445 (20), 13630 (20), 16131 (20); E. Martinez S. &
Aguilar 12435 (20); Matuda 16369 (26), 16765 (26); Max-
on et al. 6812 (14), 6820 (14); Mayo & Madison 301 (20):
McAlpin 85-33 (4); McDade s.n. (16); M
433 (15), 439 (15); McDowell 148 (20), 769 (11),
(20): McPherson 7371 (25), 9176 (15), 9829 (18), 9865
(25), 10725 (7), 10958 (14), 11129 (25),
11401 (18), 11591 ae! 11816 (2), 15037 (14);
a ‚ Aranda 10095 (2); McPherson & Merello 8143
5 (18); Meier et al. 5164 (23); Mejia & Ramirez
93): Mejia € Zanoni 6614 (23); Mena 190 (20):
Mendieta 1-10 (15), 1-101 (15), 1-121 (15):
Sc 1 5551 ( (23): 8 E Taylor 5937 (23);
al. 753 (15); Miranda, F. 7546 (20); Miyashiro s.n. (23):
Чаш D. & Chung ies (20); Montes s.n. (23);
Moore, J. W. 451 (23); Moore Jr. & Bunting 8928 (20).
8933 (20): Mora 51 Е 70 (18); Moraga 173 (20); Мо-
rales 1047 (26), 2035 (13); :
reno 15290 (26), 16421 (26), 16464 (26), 17142 (24):
Moreno & Henrich 8427 (26); Moreno & Robleto 20526
(24); Moreno & Sandino 12855 (25), 12891 (25), 12917
(25), 12955 (25), 12976 (18), 15160 (18); Mori & Bolten
7698 (15); Mori & Gracie 18717 (23); Mori & Kallunki
3591 (15). 6026 (6); Mori et al. 3817 (25), 4184 (7). 6814
(25); Murphy & Jacobs 1289 (20); Moreno, P. & J. Sandino
15160 (18 p
Nash, G. 23); Nee 9023 (16), 22595 (20), 23733
(20), 29752 20 29993 (20), 41364 (23), 99121 (20); Nee
et al. 24759 20), 26103 (20); Neill 1571 (24), 1657 (26),
3629 (24); Neill & Vincelli 3484 (12); Neill et al. 11683
(15); Nelson & Andino 16247 (24); Nelson & Cruz 9215
(20), 9291 (24); Nevling & Gómez-Pampa 1505 (20); Nic-
olson 2060 8 3), 3393 (4); Nilsson & Manfredi 505 (20):
. 311 (25), 632 (25); Noriega & H. Vasquez

I

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Ne)
N
Ке)

ГЕ
=

3 67491244 16
5), 13626 (25); Palacios & Tirado
1287 (25). 11327 (15); Paredes et al. 940 (7); Penéis, D.
633 (25); Pérez 1 (25); Pérez, J. & M. Sosa 671 (23)
Peterson 6405 (16); Peterson & Annable 6768 (15); Pfei-
fer 2124 (24), 2163 (20); Philcox 8231 (23); Picado &
Gamboa p^ (20), 138 (1); Pipoly 4479 с Pitman &
25); Pittier 2600 (15), 2715 (16
3754 (14), 3766 (22), 3838 (16), 3847 ao.
(15); Pittier & Durand s.n. (1); Plowman 14121
lanco 1485 (1: ү: 1591 (18); Polanes н p 1905 E 5:
ter et al. 4282 (15); Prance et al. 30247 (23); Prevost 3258
(23), 3382 (23), 3580 (23); Proctor posl (23), 32251
(20), 38601 (23

Quesada 51 (4 4). 175(20); Quishpe & Dávila 82 (15).

Ramamoorthy et al. 3763 (20); Raven 21532 (4); Read
: Watson 84-75 (21); Renson 266 (26); Renterfa 10680
15); Rios et al. 109 (20); Rivera 623 (20), 758 (20), 1560
: Robles, К. 815 (20), 1142 (25), 1158
(25), 1234 (2), 2090 (4); Pen et al. 2050 (25); Rodrí-
guez, A. & 2 142 (20); Rodríguez, G. 32 (20); Rod-
1 J. 2 15); так et al. 607 (23); Roldan et al.

99 (18); ae 170 6436 (16); Rose et al. 4375

А. 3); Rueda et al. 40 ee ); Rueda & Coronado 6557 (24).

Salick 8092 (12), 8 25); Sanchez 539 (2); Sanders

et al. 19322 (20): E 1248 (26); Sandoval & Chin-

Bass 995

T

chilla 352 (20); Sargent 340 (23), 643 (23); Schatz 1079
(15); Schatz & Grayum 700 (20), 701 (20). 706 (25):
Se hipp : 386 (20); Schmalzel 1212 (15); Schmalzel & Al-
verson 1199 (15); Schubert & Rogerson 619 (20); Schultes
& Cabrera 17890 (23); Schwerdtfeger 21422 (25); Seler
2389 (26), 2398 (26); Shank & Molina 4288 (25); Shat-
tuck 397 (14); Shepherd 438 (19); Simmonds s.n. (23):

Sinaca 830 (20); Sintenis, P. 2793 (23); Skute h 5328 (1):
Slane 634 (23); Smith 2239 (20); ng C. E., Jr. & H.
M. Smith 3389 (6); E hs A

al. 1059 (25); Smith, H.
Soejarto & Rentería 3556 T pa 5761 (23

14122 (15), 14556 (15), 15182 (15), 15499 (15).
(18), 19397 (15), 19488 (15); Sparrow & Brewster 108
(20); Spellman et al. 164 (20); Sperry 517 (20), 525 (20),
567 (20), ipis à mm 7700 (20), 7935 (20), 18786

—
N-
=
©
5
— 3
>
—
РЕ

327 94 (20), 36314 (25), 367: 39 ^w 1000 (2). 380: 42 (20).
‚ 44754 (20), 52702
k . 55444 (20),
9 d 63620 (20), 65041
79003 (20)
aote. 7
(20); Standley E а 8 6701 (24 ; Standley
15008 125 45206 (25), 45262 (25), 45592 (20), 4
(20), 48960 “i B (25); Stein & Hamilton 990 (6);
Stergios et al. О (23); Stern et al. 433 (15); Stevens
6027 (26), 6420 ya 7457 (24), 8044. (24), 11786 (24).
12311 (24), 13564 7 13761 (20), 23642 (11), 24251
12); Stevens et al. 17591 (26), 20998 (24), 24699 (12
Stevenson, P. 379 "d Steyermark 31763 (20), :
(20), 37153 (20), 37456 (20), 38647 (20), : 5
41699 (20), 44754 (20), 45410 (20), 45869 (20), 47684
(26), 47908 (20), 49321 (20), 49637 (26), 52070 (20).
60796 (23), 88864 (23), 91896 (23), 94331 (23); Steyer-
mark & Bunting 97728 (23), 105293 (23); 1 &
Davidse 116647 (23); Steyermark & Liesner 9] (23),
121834 (23); 5 n e Steyer-
mark et al. 100213 (23),
102036 (23), 122412 (23), 124629 (23).
127204 (23); Stimson 5277 (16); Siona 3317 (2

T

—

Qu
m"
zi

— —

745 (15); Sytsma 1658 (1 5), 1695
(15), 4398 (6); Sytsma & Andersson 457
Antonio 3006 (25).

Taylor 216 (20); Taylor, N. 48 (23); Taylor & Taylor
11660 (18); Tellez. " al. 4466 (20), 4875 (25); Thompson
128 (15), 160 (15), 441 (26), 3238 (23), 4593 (15), 4816
(15), 4874 (6), 4937 (2), 4951 (8), 5028 (18); Thorne &
Lathrop 40559 (20); Tipaz et al. 2280 (18); н 503
(25), 9961 (1), 12874 (25); Trujillo et al. 17397 (23);
Tyson 1438 (16), 1443 (15), 4632 (14), 6700 10550 Tyson
& Blum 3954 (15), 3997 (15), 3998 (14), 4099 (15); Tyson
15), 4631 (14), 4701 (16), 4834 (14).

18); gs et al. 2414.
3 (6); Sytsma &

. (20), 246 (20), 462 (1), 1355 (20), 1356
(20); Valverde 741 (13); Vanderveen 590 (20); Vasquez,
M. et al. V-907 (20); Villacorta et al. 314 (20), 408 (20);
von Wedel 1 v? е 2892 (18

Wagner, К. 558 (23); We babe et al. 12581 (24), 12624
(20), 12625 205 Wendland s.n. (26), 410 (26); White-
foord 1176 (20), 3284 (20); Whitefoord & Eddy 136 (15),
372 (25); Whitehill 8 (23); Wilbur 28249 (20), 37243 (20),
37337 (20); Wilbur & Jacobs 34819 (20), 34962 (20);
Wilbur et al. 15664 (6), 15861 (26); Williams, L. et al.

—
—

772

Annals of the
Missouri Botanical Garden

28479 (13); Witherspoon & Witherspoon 8401 (15); Won
s.n. (23); Woodbury et al. s.n. (23); 0 »»dson Jr. & Schery
861 (1); Woodson a A al. "2509.5 (25

Yanez et al. 1387 (25); Yuncker 496] (2
al. 8395 (20), 8551 (24), 8826 (20).

4); Yuncker et

Zak et al. 5383 (15), 5414 (15), 5726 (15); Zambrano
& PAS 1336 (14); Zanoni & Pimentel 23420 (23),
23456 (23); Zanoni 2 - 23113 (2 2h 251 59 (23), 27170
(23); Zapata et al. 289 (19); Zent, & S. 2189 (23);
Zuniga 216 (20

T

ANNALS OF THE MISSOURI BOTANICAL GARDEN: CHECKLIST FOR AUTHORS

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774

Annals of the
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6. Taxonomic Treatment

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—

scription,
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Bot. Gard. 86: 680. pace 5 10 0 latifolia Nees,
Syst. Laur.: 674. 1836. ги. Locality not in-
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1

Е"

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infraspecific

O

species with Da ax and
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given e following manner: lamina 36.4--82.8 X
9.

O

When relevant, nomina nuda, misapplied names, and
1 the discussion fol-

28

superfluous names are included in
lowing the description, but are not part of the formal
e y.

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text are limited to ca. 12 manuscript pa

O If there are a large number, an FR
examined is placed at the end of the paper, following

ecimens

*

the Literature Cited. It is arranged alphabetically by
collector, followed by collection number, followed by

the number of the taxon in the text. Names (including
repre )) of first and second collector are provided, “et
al.” if three or more.

m Веи are cited іп the text as follows: Additional
specimens н (or Selected specimens examined).
MEXICO. Oaxaea: Sierra San Pedro “ Talea,
12°37'N, 85°14’ W, 950--1100 m, 3 Feb.
gensen 865 (BM, G, K
status are optional but are omitted from longer lists.]
Countries are run together in the same paragraph, e. g.,
COU E ГКҮ A. Major political division: a OUN-

TRY B. Major political division: ... Se e par-

аара are used for major continental regions ain

major political divisions.

11. Specimen Vouchers and Genetic Sequences
ÛJ If the paper presents original data, associated herbar-
ium vouchers are cited. [Vouchers for seed and/or other
collections should be included where pertinent. De-
pendent on the paper, reference to the original wild

source may be required.] Vouchers are also cited from

common names and uses taken from specimen labels.

[|] Herbarium vouchers state the collector
herbarium in which the voucher is located,
annotation that the material represents the voucher for
the study in question

O Nucleic pd or protein sequences corresponding to
equal or r than 50 nucleotides are مرا‎ into
an 1 data bank, e.g., ank / EMBL. The
accession numbers are provided before мет alion.
[Long sequences (exceeding two pages) will not be rou-
tinely published.]

! accepts responsibility for establishing the ac-

and number,
and a clear

Gen

curacy of information provided.

12. Keys
LJ] Keys are clear and have been checked carefully for
consistency with the descriptions. Leads of each cou-
plet are parallel.
O Dichotomous keys are indentec
LJ Infraspecific taxa are keyed ки not in species

13. Literature Cited

О The Literature Cited contains full citations of all ref-
erences cited in the text.

C] All entries in the Literature Cited are cited in the text.

Spelling of author(s) name(s) and years of publication

have been double-checked.

All entries have been verified against original sources

especially journal titles, accents, diacritical Ard

and spelling in languages other than English

S last name,

=

O Periodicals are listed as follows: author
initial(s). t Full title of medial Journal abbreviated
as in B- . Volume: pages. No parenthetical part

numbers pee shies a are given unless each
art is paginated separa

one M dl style is followed: au-

, initial(s), second authors initial(s),

last name & es 1 initial(s), last name.
Books appear as follows: author’s last name, initial(s).

Yea pote нее Title Sarde ы Editor), 3rd

a V 1. 2. Publisher, City of Publicat

O For an Ah within a larger work, iis style is fol-

2
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=
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lowed: Author(s). Year. Name of the article. Pp. (

00 in Name of the editor(s E Full Title of Larger Pet
Publisher, City of Publica
Citations of work “in prep.,
dissertations, and similar references
sources have been eliminated or ries to a minimum.
They are not necessarily included in the Literature Cit-

ч КО theses and
to inaccessible

ed.

4. Illustrations
[See Guide to Digital Art, Allen Press through the Pub-
lication Submissions link on the opening page of http://
www.mbgpress.org

=e Electronic m are labeled with the first author's last
id“... Fig-

me, the first four letters of the taxon, an
urel.tif” ‘igure2.tif” ‘he file extension
clearly indicates what type of file it is

Scale bars appear on e A and
maps.

C] Magnifications/reductions are not indicated in cap-
ions.

[| Electronic scans may be pre-sized to fit either column
width (27, in. or ca. 68 mm) or full-page width (5% in.
or ca. 140 E T page а s should be a mini-
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LJ] Figures are mumbai in 9 numerals in the order
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lJ Photographs are prepared according to the printer re-
quirements

LJ Figures are grouped into composite plates when pos-
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[ | Edges of figures are squared.

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O

Captions provide all explanatory text. Captions are
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E

Volume 91, Number 4, pp. 525-784 of the ANNALS OF THE MISSOURI BOTANICAL GARDEN
was published on December 30, 2004.

ANNALS OF THE
MISSOURI BOTANICAL GARDEN

VOLUME 91
2004

Colophon
This volume of the ANNALS of the Missouri Botanical Garden has been set in APS Bodoni. The text
is set in 9 point type while the figure legends and literature cited sections are set in 8 point type.

This volume has been printed on 70# Vintage Gloss. This is an acid-free paper designed to have a

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in the production of the ANNALS is a proprietary method known as Permanent Binding.

The ANNALS is printed and distributed by Allen Press, Inc. of Lawrence, Kansas 66044, U.S.A.
© Missouri Botanical Garden 2004

ISSN 0026-6493

Volume 91
2004

ALBACH, DIRK C., M^. MONTSERRAT MARTÍNEZ-ORTEGA, MANFRED A. FISCHER
& MARK W. CHASE. Evolution of Veroniceae: A Phylogenetic Perspective

AL е IHSAN A. (see Suzanne I. Warwick, Ihsan A. Al-Shehbaz, Connie
Sauder, David К. Murray & Klaus Mummenhoff) 99
ARROYO, MARY T. KALIN, LOHENGRIN А. CAVIERES & ANA MARIA HUMANA.
Experimental Evidence of Potential for Persistent Seed Bank Formation
at a Subantarctic Alpine Site in Tierra del Fuego, Chile

Zi
~

BARTHLOTT, WILHELM (see Wolfgang Kiiper, Jan Henning Sommer, Jon C. Lov-
ett, Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva
Angéle Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm
Barthlott) 525
BEENTJE, HENK JAAP (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lov-
ett, Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva
Angèle Rosine Van Rompaey, Cyrille Chatelain, Marc Sosef & Wilhelm

Barthlott) 525
BERNHARDT, PETER (see Peter Goldblatt, Ingrid Nänni, Peter Bernhardt & John
C. Manning) 6 186
BRADFORD, JASON C. (see Patrick W. Sweeney, Jason C. Bradford & Porter P.
Lowry П) 206
BROWN, GREGORY K. (see Ana Paula Gelli de Faria, Tánia Wendt € Gregory
K. Brown) 303
Bruyns, P. V. & C. Klak. Revision of the Madagascan Endemic Stapelianthus
(Apocynaceae) Based on Molecular and Morphological Characters — 410
BURGESS, K. S., J. SINGFIELD, V. MELENDEZ & Р. G. KEVAN. Pollination Biology
of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico —— 346
CARDONA, FELIPE. Synopsis of the Genus e (Araceae) in Colombia
448
CATALAN, PILAR (see Pedro Torrecilla, José-Angel López-Rodríguez & Pilar
CARS ss N ышы ыл. 124
CAVIERES, LOHENGRIN A. (see Mary Т. Kalin Arroyo, Lohengrin A. Cavieres
& Ana Marfa Humaña) ЙИТИ 357
CHASE, MARK W. (see Dirk C. Albach, М", Montserrat Martínez-Ortega, Man-
fred A. Fischer & Mark W. Chase) 275
CHATELAIN, CYRILLE (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lov-
ett, Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva
Angèle Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm
Barthlott) 525
CHEN, J. (see R. J. Henny, D. J. Norman & J. Chen) 464.

CHIANG, TZEN-YUH, Kuo-HsinG Hunc, TSAI-WEN Hsu & WEN-LUAN WU.

Lineage Sorting and Phylogeography in Lithocarpus formosanus and L.

dodonaeifolius (Fagaceae) from Taiwan 207

CLINEBELL, RICHARD R., II. ANGELA CROWE, DAVID P. GREGORY & PETER С.
Носн. Pollination Ecology of Gaura and didi (Onagraceae, Tribe
Onagreae) in Western Texas, U. S. A.

COELHO, Marcus A. NADRUZ (see Eduardo G. Gonçalves, Élder A. S. Paiva
& Marcus A. Nadruz Coelho) ——
CRISCI, JORGE V. (see Liliana Katinas, Jorge V. Crisci, Warren L. Wagner &
Peter C. Hoch) |...
Croat, THOMAS B. VIII International Aroid Conference, Missouri Botanical
Garden, St. Louis, 9-11 August 1999: Introduction

CROAT, THOMAS B. (see Guanghua Zhu & Thomas B. Croat)

Croat, THOMAS B. Revision of Dieffenbachia (Araceae) of Mexico, Central
America, and the West Indies 0

CrosBY, MARSHALL R. & JAMES C. SOLOMON. Statistical Summary of Some of

the Activities in the Missouri Botanical Garden Herbarium, 200:
CROWE, ANGELA (see Richard R. Clinebell П, кш Crowe, David Р. Gregory
& Peter C. Hoch) s

DENHAM, SILVIA S. (see Osvaldo Morrone, Silvia S. Denham € Fernando О.
Zuloaga) .

FARIA, ANA PAULA GELLI DE, TANIA WENDT & GREGORY K. BROWN. Cladistic
ina а of Aechmea (Bromeliaceae, Bromelioideae) and Allied Gen-
era . А ESAS ES ARIETE Ie eR T 8

FINOT, VICTOR L., PAUL M. PETERSON, ROBERT J. SORENG & FERNANDO O.
ZULOAGA. A Revision of Trisetum, Peyritschia, and ii nd tale (Po-
aceae: Pooideae: Aveninae) in Mexico and Central America —

FISCHER, MANFRED A. (see Dirk C. Albach, Ma. Montserrat Martínez-Ortega,
Manfred A. Fischer & Mark W. Chase) .

GASKIN, JOHN F., FARROKH GHAHREMANI-NEJAD, DAO-YUAN ZHANG & JASON
P. LONDO. A Systematic Overview of Frankeniaceae and Tamaricaceae
from Nuclear rDNA and Plastid Sequence Data

GHAHREMANI-NEJAD, FARROKH (see John F. Gaskin, Farrokh Ghahremani-ne-
jad, Dao-yuan Zhang & Jason P. Londo)

GOLDBLATT, PETER, INGRID NÄNNI, PETER BERNHARDT & JOHN С. MANNING,
Floral Biology of Hesperantha (Iridaceae: Crocoideae): How Minor Shifts
in Floral Presentation Change the Pollination System —

GONÇALVES, EDUARDO С. Araceae from Central Brazil: Comments on Their
Diversity and Biogeography — —! ꝶʒ!!!!!12n21—

GONÇALVES, EDUARDO G., ELDER A. S. Paiva & MARCUS A. NADRUZ COELHO.
A Preliminary Survey of Petiolar Collenchyma in the Araceae

GOULD, KATHERINE R. & LENA SrRUWE. Phylogeny and Evolution of Symbo-
lanthus and Wurdackanthus (Gentianaceae-Helieae) in the Guayana
Highlands and Andes, Based on Ribosomal 58-NTS sequences ——

GREGORY, DAVID Р, (see Richard R. Clinebell H, Angela Crowe, David Р.
Gregory & Peter С. Hoch)

303

401

401

438

369

GUNN, BEE F. The Phylogeny of the Cocoeae (Arecaceae) with Emphasis on
Cocos nucifera

HAEVERMANS, THOMAS, PETRA HOFFMANN, PORTER P. Lowry Il, JEAN-NOEL
LABAT & EMILE RANDRIANJOHANY. Phylogenetic Analysis of the Mada-
gascan Euphorbia subgenus Lacanthis Based on ITS Sequence Data

Henny, К. J., D. J. NORMAN & J. CHEN. Progress in Ornamental Aroid Breed-
ing Research

Носн, PETER C. (see Liliana Katinas, Jorge V. Crisci, Warren L. Wagner &
Peter C. Hoch) ——
HOCH, PETER C. (see Richard К. Clinebell II. Angela Crowe, David P. Gregory
& Peter C. Hoch) —
HOFFMANN, PETRA (see Thomas Haevermans, Petra Hoffmann, Porter P. Lowry
II. Jean-Noël Labat & Emile Randrianjohany) .

HONG Dr-YUAN & PAN Kar-Yu. A Taxonomic Revision of the Paeonia an-
omala Complex (Paeoniaceae) —

HONG, S.-P. (see L. P. Ronse De Craene, S.-P. Hong & E. F. Smets) —

Hsu, TsAr-WEN (see Tzen-Yuh Chiang, Kuo-Hsing Hung, Tsai-Wen Hsu &
Wen-Luan Wu)

HUMANA, ANA María (see Mary Т. Kalin Arroyo, Lohengrin A. Cavieres &
Ana María Humana

Hunc, Kvo-HsiNc (see Tzen-Yuh Chiang, Kuo-Hsing Hung, Tsai-Wen Hsu &
Wen-Luan Wu)

JANSEN, STEVEN (see Frederic Lens, Kathleen A. Kron, James L. Luteyn, Erik

Smets & Steven Jansen) |

KATINAS, LILIANA, JORGE V. CRISCI, WARREN L. WAGNER & PETER С. HocH.
Geographical Diversification of Tribes Epilobieae, Gongylocarpeae, and
Onagreae (Onagraceae) in North America, Based on Parsimony Analysis
of Endemicity and Track Compatibility Analysis —

KEATING, RICHARD C. Vegetative Anatomical Data and Its Relationship to a
Revised Classification of the Genera of Araceae

KEATING, RICHARD C. Systematic Occurrence of Raphide Crystals in Araceae

Kevan, P. С. (see K. S. Burgess, J. Singfield, V. Melendez & P. G. Kevan) —
KLAK, C. (see P. V. Bruyns & C. Ka

KRON, KATHLEEN A. (see Frederic Lens, Kathleen A. Kron, James L. Luteyn,
Erik Smets & Steven Jansen) 1.

KUPER, WOLFGANG, JAN HENNING SOMMER, JON C. LOVETT, JENS MUTKE,
HANS PETER LINDER, HENK JAAP BEENTJE, RENAAT SYLVA ANGÈLE RO-
SINE VAN ROMPAEY, CYRILLE CHATELAIN, MARC SOsEF & WILHELM
BARTHLOTT. Africa's Hotspots of Biodiversity Redefined — ——
LABAT, JEAN-NOEL (see Thomas Haevermans, Petra Hoffmann, Porter P. Lowry
II. Jean-Noél Labat & Emile Randrianjohany)

505

207

566

л
N
л

LENS, FREDERIC, KATHLEEN A. KRON, JAMES L. LUTEYN, ERIK SMETS & STEV-
EN JANSEN. Comparative Wood Anatomy of the Blueberry Tribe (Vacci-
nieae, Ericaceae s.l.)

LIEDE, SIGRID & ULRICH Meve. Revision of Metastelma (Apocynaceae—Ascle-
piadoideae) in Southwestern North America and Central America
LINDER, HANS PETER (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lov-
ett, Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva
Angèle Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm
Barthlott)
LONDO, JASON P. (see John F. Gaskin, Farrokh Ghahremani-nejad, Dao-yuan
Zhang & Jason P. Londo) —
LÓPEZ-RODRÍGUEZ, JOSE-ANGEL (see Pedro Torrecilla, José-Angel López-Rod-
ríguez & Pilar Catalán) EEES

LORENCE, DAVID H. & GERMINAL ROUHAN. A Revision of the Mascarene Spe-
cies of Elaphoglossum (Elaphoglossaceae)

Loverr, JON C. (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lovett,
Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva Angele
Rosine Van чан Cyrille Chatelain, Mare Sosef & Wilhelm Barthlott)

LOWRY, PORTER P., II (see Thomas Haevermans, Petra Hoffmann, Porter P.
Lowry II, Jean-Noël Labat & Emile Randrianjohany)

LOWRY, PORTER P., II (see Gordon McPherson & Porter P. Lowry II) ———
Lowry, PORTER P., H (see Patrick W. cia Jason С. Bradford & Porter P.
Lowry Il)

LUTEYN, JAMES L. (see Frederic Lens, Kathleen A. Kron, James L. Luteyn,
Erik Smets & Steven Jansen) . ее

MANNING, JOHN С. (see Peter Goldblatt, Ingrid N Nünni, Peter Bernhardt & John
C. Manning) — A 8
MARTÍNEZ-ORTEGA, M*. MONTSERRAT (see Dirk C. Albach, M*. Montserrat
Martínez-Ortega, Manfred A. Fischer & Mark M. Chase) |...
McPHERSON, GORDON & PORTER P. Lowry Il. Hooglandia, a Newly Discov-
ered Genus of Cunoniaceae from New Caledonia
MELENDEZ, V. (see К. S. Burgess, J. Singfield, V. Melendez & P. С. Kevan) .
MEVE, ULRICH (see Sigrid Liede & Ulrich Meve)
MORRONE, OSVALDO, SILVIA S. DENHAM & FERNANDO O. ZULOAGA. Revisión
Taxonómica del Género Paspalum Grupo Eriantha (Poaceae, Panicoideae,

Paniceae/

MUMMENHOFF, KLAUS (see Suzanne I. Warwick, Ihsan A. Al-Shehbaz, Connie
A. Sauder, David F. Murray & Klaus Mummenhoff)
MURRAY, Одур F. (see Suzanne I. Warwick, Ihsan A. Al-Shehbaz, Connie A.
Sauder, David F. Murray & Klaus Mummenhoff) e

566

124

536

566

186

MUTKE, JENS (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lovett, Jens
Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva Angéle
Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm Barthlott)

NANNI, INGRID (see Peter Goldblatt, Ingrid Nänni, Peter Bernhardt & John C.
Manning) —
Norman, D. J. (see R. J. Henny, D. J. Norman & J. Chen)

Paiva, ÉLDER А. S. (see Eduardo С. ia nn Elder A. S. Paiva & Marcus
A. Nadruz Coelho)

PAN Kar-Yu (see Hong De-Yuan & Pan Kai-Yu) —
PETERSON, PAUL M. (see Victor L. Finot, Paul M. Peterson, Robert J. Soreng
& Fernando O. Zuloaga)
RANDRIANJOHANY, EMILE (see Thomas Haevermans, Petra Hoffmann, Porter P.
Lowry II. Jean-Noël Labat & Emile Randrianjohany)

ROMPAEY, RENAAT SYLVA ANGELE ROSINE VAN (see Wolfgang Kiiper, Jan Hen-
ning Sommer, Jon С. Lovett, Jens Mutke, Hans Peter Linder, Henk Jaap
Beentje, Renaat Sylva Angéle Rosine Van Rompaey, Cyrille Chatelain,
Marc Sosef & Wilhelm Barthlott) С. ЛИТОГО

Ronse DE CRAENE, L. P., S.-P. HONG & E. F. Smers. What Is the Taxonomic
Status of Polygonella? Evidence of Floral M

Ї OJ
ROUHAN, GERMINAL (see David H. Lorence & Germinal Rouhan)

SAUDER, CONNIE А. (see Suzanne I. Warwick, Ihsan A. Al-Shehbaz, Connie A.
Sauder, David F. Murray & Klaus Mummenhoff)

SINGFIELD, J. (see K. S. Burgess, J. Singfield, V. Melendez & P. С. Kevan) —
Smets, Е. F. (see L. P. Ronse De Craene, S.-P. Hong & E. F. Smets) —

SMETS, ERIK (see Frederic Lens, Kathleen A. Kron, James L. Luteyn, Erik
Smets & Steven Jansen)

SOLOMON, JAMES C. (see Marshall R. Crosby & James C. Solomon) ————

SOMMER, JAN HENNING (see Wolfgang Kiiper, Jan Henning Sommer, Jon €
Lovett, Jens Mutke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva
Angéle Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm
Barthlott)

SORENG, ROBERT J. (see Victor L. Finot, Paul M. Peterson, Robert J. Soreng
¿ Fernando O. Zuloaga

SosEF, MARC (see Wolfgang Küper, Jan Henning Sommer, Jon C. Lovett, Jens
utke, Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva Angéle
Rosine Van Rompaey, Cyrille Chatelain, Mare Sosef & Wilhelm Barthlott)

STRUWE, LENA (see Katherine R. Gould & Lena Struwe)

SWEENEY, PATRICK W., JASON C. BRADFORD & PORTER P. Lowry II. Phylo-
genetic Position of the New Caledonian Endemic Genus Hooglandia (Cu-
noniaceae) as Determined by Maximum Parsimony Analysis of Chloro-

plast DNA

247

2606

TORRECILLA, PEDRO, JOSE-ANGEL LOPEZ-RODR{GUEZ & PILAR CATALÁN. Phy-
logenetic Relationships of Vulpia and Related Genera (Poeae, Poaceae)
Based on Analysis of ITS and trnL-F Sequences

WAGNER, WARREN L. (see Liliana Katinas, Jorge V. Crisci, Warren L. Wagner
& Peter C. Hoch) ·f᷑ꝛ—— —
WARWICK, SUZANNE I., IHSAN А. AL-SHEHBAZ, CONNIE A. SAUDER, DAVID F.
MURRAY & KLAUS MUMMENHOFF. Phylogeny of Smelowskia and Related
Genera (Brassicaceae) Based on Nuclear ITS DNA and Chloroplast trnL

Intron DNA Sequences

WENDT, TANIA (see Ana Paula Gelli de Faria, Tania Wendt & Gregory K.

Brown ене
Wu, WEN-LuAN (see Tzen-Yuh Chiang, Kuo-Hsing Hung, Tsai-Wen Hsu &
Wen-Luan Wu)
ZHANG, DAO-YUAN (see John F. Gaskin, Farrokh Ghahremani-nejad, Dao-yuan

Zhang & Jason P. Londo) ——

ZHU, GUANGHUA & THOMAS B. CROAT. Revision of Dracontium (Araceae) —
ZULOAGA, FERNANDO O. (see Victor L. Finot, Paul M. Peterson, Robert J.
Soreng & Fernando O. Zuloaga) -............
ZULOAGA, FERNANDO O. (see Osvaldo Morrone, Silvia S. Denham & Fernand
O. Zuloaga)

ШОТ

www.mbgpress.org

CONTENTS

Africa’s Hotspots of Biodiversity Redefined
Wolfgang Kiiper, Jan Henning Sommer, Jon C. Lovett, Jens Mutke,

Hans Peter Linder, Henk Jaap Beentje, Renaat Sylva Angèle

Rosine Van Rompaey, Cyrille Chatelain, Marc Sosef & Wilhelm Barthlott

A Revision of the Mascarene Species of Elaphoglossum (Elaphoglossaceae) 7777

avid Н. Lorence & Germinal Rouhan

Comparative Wood Anatomy of the Blueberry Tribe (Vaccinieae, Ericaceae s.l.)
Frederic Lens, Kathleen А. Kron, James L. Luteyn,
Erik Smets & Steven Jansen

Revision of Dracontium (Araceae) Guanghua Zhu & Thomas B. Croat
Revision of Dieffenbachia (Araceae) of Mexico, Central America, and the West Indies ——
| Thomas B. Croat

Checklist for Authors
Index for Volume 91

Cover illustration. Trisetum ligulatum Finot & Zuloaga, drawn by Vladimiro Dudás.